Einar Ringø
Xuemei Li2
Hien van Doan
Koushik Ghosh- 1Norwegian College of Fishery Science, Faculty of Bioscience, Fisheries and Economics, UiT The Arctic University of Norway, Tromsø, Norway
- 2Key Laboratory of Freshwater Biodiversity Conservation, Ministry of Agriculture of China, Yangtze River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Wuhan, China
- 3Department of Animal and Aquatic Sciences, Faculty of Agriculture, Chiang Mai University, Chiang Mai, Thailand
- 4Aquaculture Laboratory, Department of Zoology, The University of Burdwan, Burdwan, India
Growing demands stimulate the intensification of production and create the need for practices that are both economically viable and environmentally sustainable. As European Union banned the use of antibiotics in production in 2003, several alternative treatments have been suggested, including probiotics. The first probiotic study in aquaculture was published in 1986, and since then probiotics have been considered as a beneficial tool in this industry. Today current evidence suggests that administration of certain probiotic strains might be able to enhance growth rate, improve the welfare of different fish species by modulating gut microbiota, improve physiological functions, such as metabolism, digestion, immunity, stress tolerance, intestinal histology, and disease resistance. Even though lactic acid bacteria and Bacillus spp. are the most frequently used probiotics in aquaculture, numerous studies have been published on other interesting probiotics. Therefore, the purpose of this paper is to summarize, comment, and discuss the current knowledge related to the effects of Aeromonas, Aliivibrio, Alteromonas, Arthrobacter, Bifidobacterium, Brochothrix, Clostridium, Enterovibrio, Kocuria, Microbacterium, Micrococcus, Paenibacillus, Phaeobacter, Pseudoalteromonas, Pseudomonas, Rhodococcus, Rhodopseudomonas, Rhodosporidium, Roseobacter, Shewanella and Vibrio as probiotics in finfish aquaculture, and present general information on their presence in the gastrointestinal tract of finfish. Moreover, some considerations for future studies are also indicated.
Introduction
By 2025, aquaculture is expected to play a leading role in the global supply of fish. However, the growth of this industry could be considerably hampered by failures to predict, avoid, and contain infections. Unsurprisingly, the intensification of aquatic production has led to a significant increase in the frequency of disease and a growing inefficiency among the antibiotics used to treat these.
Antibiotics have been used in aquaculture for more than 50 years (Shamsuzzaman and Kumar, 2012), and previously the most common method for dealing with the occurrence of bacterial infections was the administration of antibiotics (Cabello, 2006; Cabello et al., 2020; Lulijwa et al., 2020), and the rapid growth of for example the Chilean salmon industry was accompanied by intensive use of antibiotics. However, as antibiotic administrations became the target of increasing public criticism and political controversy, Sweden was the first country in Europe, to ban the use of antimicrobial growth promoters as early as 1986. In 2003, European Union stated in Regulation (EC) No. 1831/2003; “Antibiotics, other than coccidiostats or histomonostats, shall not be authorized as feed additives”. However, recent findings have revealed that mono- (e.g., Gudmundsdottir and Bjornsdottir, 2007) and polyvalent vaccines (e.g., Tobar et al., 2015) are effective for disease control in aquaculture, especially for salmonids. However, for many Chinese and Indian finfish-, shellfish- and cucumber species, vaccines are not available, and will hardly be available soon. However, there are several alternative treatment options available; phytobiotics, phage therapy, bacterial membrane vesicles (e.g., Jan, 2017; Tandberg et al., 2019; Mertes et al., 2021), quorum sensing interference, postbiotics (secreted by live bacteria, or released after bacterial lysis; Ang et al., 2020; Cuevas-González et al., 2020; Teame et al., 2020), postbiotics in combination with prebiotics, paraprobiotics (cell wall components; Taverniti and Guglielmetti, 2011; Choudhury and Kamilya, 2019; Nataraj et al., 2020), pro-, pre- and synbiotics. However, Cheng et al. (2014) argue that these “so-called alternatives” are not ideal antibiotics replacers.
According to Bermudez-Brito et al. (2012), “Probiotics are live microorganisms that provide health benefits to the host when ingested in adequate amounts”. The probiotic concept is primarily based on the assumption that direct feeding of microbial cultures possesses beneficial effects on growth performance, digestive processes, the immune system and animal health. The use of probiotics gained attention within aquaculture in the mid 1980s (Kozasa, 1986), and since then numerous reviews papers have been published (e.g., Gatesoupe, 1999; Irianto and Austin, 2002a; Merrifield et al., 2010; Dimitroglou et al., 2011; Hoseinifar et al., 2018; Ringø et al., 2018; Wang et al., 2019a; Hoseinifar et al., 2020; Hu et al., 2020; Ringø et al., 2020a; Ringø et al., 2020b; Yao et al., 2020; Nayak, 2021; van Doan et al., 2021). In this context, it is also worth mention that administration of antibiotics lead to their accumulation in the tissues (Chen et al., 2020a), emergence of antimicrobial resistant bacteria in the environment (e.g., Marti et al., 2014; Chen et al., 2020a; Lulijwa et al., 2020), modulation of the gut microbiota (dysbiosis) (e.g., Ringø et al., 2016; Kim et al., 2019; Legrand et al., 2020), suppression of certain gut bacteria (Saettone et al., 2020), and increased abundance of intestinal bacteria that act as reservoirs for antibiotic resistance genes (Salyers et al., 2004; Saenz et al., 2019). In addition, modulation of the gut microbiota to an undesirable community can induce mucosal inflammation (Tamboli et al., 2004; Turroni et al., 2014). Furthermore, many antibiotics currently used in aquaculture are, or are closely related to agents used to treat bacterial diseases in humans, which makes their uncontrolled application in animal production an enormous risk to host health. It is thus clear that new methods to control aquatic infections is required.
Among the probiotic bacteria used in aquaculture are lactic acid bacteria (LAB) and Bacillus most frequently used (e.g., Ringø et al., 2018a; Kuebutornye et al., 2019; Soltani et al., 2019; Ringø et al., 2020a; Nayak, 2021; James et al., 2021; van Doan et al., 2021). However, in addition to LAB and bacilli are numerous probiotics such as Aeromonas, Alteromonas, Arthrobacter, Bifidobacterium, Brochothrix, Clostridium, Kocuria, Microbacterium, Micrococcus, Paenibacillus, Phaeobacter, Pseudoalteromonas, Pseudomonas, Rhodococcus, Rhodopseudomonas, Rhodosporidium, Roseobacter, Shewanella and Vibrio used.
The use of probiotics is an alternative approach to reduce pathogen adherence and colonization in larval-, fry- and juvenile intestines by modulating the intestinal microbiota with beneficial bacteria. They can be added to the diet or water in order to enhance the proportion of health-promoting bacteria in the gut. An advantage of this method is that it can be implemented during the early stages of development when vaccination by injection is impractical.
The review of Irianto and Austin (2002a); Tapia-Paniagua et al. (2012); De et al. (2014); Newaj-Fyzul et al. (2014), Tan et al. 2020), Cámara-Ruiz et al. (2020); Hayatgheib et al. (2020), and van Doan et al. (2021) presented some information on administrations of the probiotic bacteria discussed in the present study, and to avoid duplication with that presented in the above mention reviews, these studies are only briefly presented in Tables.
The present review address to present an overview of interesting probiotic bacteria, not LAB and bacilli, with focus on growth performance, modulation of the gut microbiota, gut histology, effect on immunesystem, and disease resistance in finfish. Furthermore, some general information is presented on the probiotics discussed, and their presence in the GI tract of finfish.
Administration and Mode of Actions
Probiotic administration has been described in several reviews (e.g., Verschuere et al., 2000; Irianto and Austin, 2002a; Villamil et al., 2010; Dawood and Koshio, 2016; Kumar et al., 2016; Hoseinifar et al., 2018; Jahangiri and Esteban, 2018; Ringø et al., 2020a; Vargas-Albores et al., 2021), and in order to avoid overlaps, the administration methods are only briefly presented.
i) Oral administration via diet or water/bath, ii) Administration of several probiotics in combination (Fuller, 1989; Kesarcodi-Watson et al., 2012; Melo-Bolivar et al., 2021), iii) Inactivated bacteria, iv) Spores, v) Culturing, and added to feed as freeze-dried cultures, which sometimes are coated with lipids, vi) Encapsulation e.g., by calcium alginate beads (e.g., Rosas-Ledesma et al., 2012; Cordero et al., 2015; Prado et al., 2020), vii) Lyophilization, viii) Administration – continuously or regular intervals, but are the probiotics permanently colonisers in the GI tract, ix) Co-administration of probiotics with prebiotics or plant products, and x) Host specificity, or strains from other species or commercial probiotics (Lazado et al., 2015; van Doan et al., 2020).
The modes of action of probiotics are well discussed, and several hypotheses have been suggested (e.g., Irianto and Austin, 2002a; Prado et al., 2010; Kumar et al., 2016; Zorriehzahra et al., 2016; Wang et al., 2017; de Melo Pereira et al., 2018; Hoseinifar et al., 2018; Chauhan and Singh, 2019; Ran et al., 2021), and according to these reviews the modes of action are: a) competitive adhesion of probiotic microorganisms to epithelial receptors may prevent the attachment of pathogenic bacteria (rational behind “competitive exclusion”), b) aggregation of probiotics and pathogenic bacteria, c) competition for nutrients between probiotic and undesired bacteria, d) increased synthesis of lactic acid and reduction of intestinal pH, e) production of specific antibacterial substances, f) reduced production of toxic amines and decrease of ammonia level in the GI tract, g) beneficial effects on the intestinal immune system, h) interference with quorum sensing, i) bioremediator, j) improved defense against bacterial and viral infections, k) alleviate negative effects induced by crowding stress, and l) antioxidant properties.
Gram-Negatives
In Table 1 are the beneficial effects of Gram-negative probiotic bacteria used in finfish aquaculture revealed. In addition, some vital information is presented from in vitro studies.
Table 1 Effect of Gram-negative bacteria on growth performance, gut health, immune system and disease resistance in finfish, and some in vitro studies.
Acinetobacter
Acinetobacter belong to Gammaproteobacteria, is oxidase-negative, aerobic coccobacilli with twitching motility. They are isolated from the GI tract of finfish (e.g., Ringø et al., 2006a; Navarrete et al., 2013; Liu et al., 2019; Wang et al., 2020a), but their use as probiotics in finfish are less investigated (Bunnoy et al., 2019a), and as a part in multi-strain probiotic supplementation (Li et al., 2019a).
In a study with bighead catfish (Clarias macrocephalus; 150g), Bunnoy et al. (2019a) used an Acinetobacter originally isolated from skin mucus of bighead catfish revealing strong antibacterial activity against several freshwater pathogens in vitro (Bunnoy et al., 2019b). After 15- and 30-days administration, phagocytic index, phagocytic-, lysozyme-, and respiratory burst activity, and alternative complement pathway significantly enhanced, and upregulation of immune-related genes was observed. After 30 days administration, increased resistance was observed following intraperitoneal injection with Aeromonas hydrophila. The main reason why Acinetobacter species have little been used as probiotics in finfish, may be due to reports on opportunistic fish pathogenic agents within the genus.
Aeromonas
Aeromonas is facultative anaerobic, rod-shaped bacteria. Even though Aeromonas are mainly associated with diseases (Feckaninova et al., 2017), there are present in the GI tract of healthy finfish (e.g., Ringø et al., 1997; Navarrete et al., 2013; Chen et al., 2014; Abdelhamed et al., 2019). In finfish, information is available on the use of Aeromonas as probiotics (Irianto and Austin, 2002b; Lategan et al., 2004; Brunt and Austin, 2005; Makridis et al., 2005; Brunt et al., 2007; Brunt et al., 2008; Makridis et al., 2008; Pieters et al., 2008; Abbass et al., 2010; Wu et al., 2015; Hao et al., 2017), as well as a part of multi strains probiotics supplementation; Aeromonas veronii in combination with Flavobacterium sasangense (Chi et al., 2014).
Irianto and Austin (2002b) indicated that feed supplemented with A. hydrophila for 7 and 14 days led to better survival rate of rainbow trout (Oncorhynchus mykiss) following challenge with Aeromonas salmonicida. In contrast, Makridis et al. (2005) revealed no clear effect on survival of gilthead sea bream (Sparus aurata) larvae exposed to 6 x 105 Aeromonas mL-1.
Saprolegina paracitica (saprolegniosis; caused by fungal infections) is reported in silver perch (Bidyanus bidyanus), and Lategan et al. (2004) revealed that administration of Aeromonas media strain A199 to the tank water of silver perch halted the outbreak. In three later studies using Aeromonas sobria GC2 as probiont to rainbow trout, Brunt and Austin (2005) and (2008); Brunt et al. (2007) revealed enhanced survival after challenge with a range of pathogens. Similarly, Pieters et al. (2008) displayed that dietary inclusion of A. sobria protected rainbow trout against surface infections and against a eukaryotic pathogen, Ichthyophthirius multifiliis. Abbass et al. (2010) evaluated intraperitoneal and intramuscular injections of subcellular component of A. sobria GC2 to rainbow trout and revealed protection against Yersinia ruckeri.
Even though, diseases caused by A. veronii in freshwater fish are reported (e.g., Liu et al., 2018), the bacterium has been used as probiotic supplement. A dietary supplementation of A. veronii isolated from grass carp (Ctenopharyngodon idella) was administrated to grass carp, 108 CFU g-1, for 28 days and challenged with A. hydrophila (Wu et al., 2015). A significant increase of respiratory burst, phagocytic and lysozyme activities, and upregulation of immune related genes (IL-8, IL-1β, lysozyme-C and TNF-α), and resistance against A. hydrophila were observed. Modulation of the gut microbiota of grass carp by A. veronii administration was revealed by Hao et al. (2017), as Brevundimonas was the abundant genus in the GI tract, while Lactococcus, Pseudomonas and Vibrio decreased, and Flavobacterium and Lactococcus was not detected in probiotic administrated fish compared to control fed fish.
Alcaligenes
A genus of rod-shaped, motile, aerobic bacteria, and some strains of Alcaligenes are capable of anaerobic respiration in the presence of nitrate or nitrite. The genus does not use carbohydrates. Strains of Alcaligenes are reported in the intestinal tracts of vertebrates as well as finfish (e.g., Ringø, 1993; Navarrete et al., 2013; Sedlacek et al., 2016; Karlsen et al., 2017).
A decapeptide (cyclo‐(l‐Pro‐Gly)5) from Alcaligenes faecalis revealed immunostimulatory activities in a study with crucian carp (Carassius carassius) (Wang et al., 2011), and a challenge experiment displayed that fish injected with the decapeptide significantly improved survival (87.0%) compared with the control (54.6%) after infection with live A. hydrophila. An Alcaligenes sp. at inclusion level of 108 CFU g-1 feed, was fed to Malaysian Mahseer (Tor tambroides) for 90 days (Asaduzzaman et al., 2018). Weight gain, gut histology (villi height, villi with and villi area), and production of short chain fatty acids (SCFAs) significantly improved, and modulation of the gut microbiota Wang et al. (2020a) conducted a three-month feeding trial with Nile tilapia (Oreochromis niloticus) to determine the effect of Alcaligenes faecalis Y311 supplementation and revealed increase of alkaline phosphatase activities in gill and intestine. Probiotic administration did not affect the dominant bacteria but affected the relative abundance of some low abundance bacteria, Methyloparacoccus, Enterococcus, Limnohabitans, Tepidimonas and Cetobacterium in skin, gill and intestine. One interesting finding was that the relative abundance of Acinetobacter, potential pathogen, decreased in the gut by A. faecalis Y311 administration.
Alteromonas
Genus Alteromonas are facultative anaerobic bacteria, and in the absence of oxygen, the genus possess capabilities to use of a variety of other electron acceptors for respiration, for example trimethylamineoxide (Ringø et al., 1984). The genus is isolated from the GI tract of finfish (e.g., Akimoto et al., 1990; Jiang et al., 2018; Fonseca et al., 2019), and some information is available on the use of Alteromonas as probiotic supplement in shellfish (Ringø, 2020), but less information is available on their use as probiotics in finfish aquaculture (Mladineo et al., 2016). Mladineo et al. (2016) revealed improved phagocytic activity, respiratory burst, and gene expression of lysozyme, Mx protein, caspase 3, TNF-a, and IL-10, by Alteromonas sp. administrated to European sea bass (Dicentrarchus labrax).
Chromobacterium
Chromobacterium is a facultative anaerobic, motile and non-sporing coccobacillus, present in the GI tract of finfish (Ziólkowska et al., 2009; Zhou et al., 2016).
In a recent study, Yi et al. (2019) evaluated the effect of administration of a Chromobacterium aquaticum isolated from lake water with bacteriocin-like activity on zebrafish (Danio rerio) and revealed improved hepatic mRNA expression of carbohydrate metabolism-related genes, including glucokinase, hexokinase, glucose-6-phosphatase and pyruvate kinase, and growth-related genes, induced effect on innate immune-related genes and enhanced resistance against A. hydrophila and Streptococcus iniae by probiotic administration.
Enterobacter
Genus Enterobacter is rod shaped, facultative anaerobic, non-spore-forming bacteria and belong to family Enterobacteriaceae. During the last years, information has become available showing the presence of Enterobacter in intestine of finfish (e.g., Tapia-Paniagua et al., 2014a; Tapia-Paniagua et al., 2019; Terova et al., 2019; Nguyen et al., 2020).
Burbank et al. (2011) reported administration of Enterobacter strain PIC15 and Enterobacter amnigenus to rainbow trout for 7 days and revealed significant improved resistance against Flavobacterium psychrophilum. Furthermore, as both probiotic strains were isolated from the GI tract, this finding may indicate their ability to colonize the GI tract. Kenyi cichlid (Maylandia lombardoi) fed 60 days on an Enterobacter cloacae isolated from curd revealed enhanced growth, respiratory burst activity, and modulated the gut microbiota (Girijakumari et al., 2018). Moreover, it is of interest to notice that dietary administration of Enterobacter cloacae in combination with Bacillus mojavensis at 108 CFU g−1 to rainbow trout for 60 days improved protection against Y. ruckeri, as survival rate increased to 99.2% vs. 35% in the control group (Capkin and Altinok, 2009).
Phaeobacter
Genus Phaeobacter belongs to family Rhodobacteraceae and was first suggested by Martens et al. (2006). Phaeobacter is important as a carbon and sulfur metabolizer, and a biofilm former and antibiotic tropodithietic acid producer (TDA) a sulfur-containing compound (Porsby et al., 2008; Dittmann et al., 2020). Most of the cultured strains of Phaeobacter are isolated from aquatic environments, and from the intestine of finfish (Hjelm et al., 2004; Planas et al., 2004; Terova et al., 2019). Information is available on its use as probiotic, as well as a part of multi strains probiotics supplementation with Bacillus pumilus (Schmidt et al., 2017), and Phaeobacter inhibens in combination with vibriophage KVP40 (Rasmussen et al., 2019).
In a previous review, Dimitroglou et al. (2011) discussed probiotic administration of Phaeobacter in Mediterranean finfish, and in order to avoid overlaps we recommend readers with interest to have a closer look at the papers discussed in the above mention review.
Phaeobacter gallaeciensis isolated from seawater of scallop cultures and administrated to Atlantic cod (Gadus morhua) larvae enhanced survival towards Vibrio anguillarum serotype 01 (D’Alvise et al., 2012). In a later study with Atlantic cod larvae, improved resistance against V. anguillarum 02α was noticed when Phaeobacter sp. isolated from turbot hatchery was added into well dishes at 107 CFU mL-1 (D’Alvise et al., 2013). Based on their results, the author suggested that Phaeobacter was a promising probiont in marine larval culture, and that TDA contribute to its probiotic effect as a mutant of P. gallaeciensis did not reduce V. anguillarum numbers.
Planas et al. (2004) revealed that Phaeobacter 27-4 administration improved survival against V. anguillarum and detected 27-4 in GI lumen of turbot (Scophthalmus maximus) when the probiont was administrated to the larvae incorporated in rotifers, but 27-4 did not colonize the larval gut and intestinal epithelium.
A Phaeobacter strain isolated from turbot hatchery, grown on ceramic biofilter (probiofilter) revealed resistance against V. anguillarum, improved seawater quality by decreasing turbidity, but the bacterial diversity in larval turbot (Psetta maxima) gut was unchanged (Prol-García and Pintado, 2013). In a recent study, Dittmann et al. (2020) studied administration of a TDA producing P. inhibens strain DSM17395 isolated from mariculture environment to turbot larvae, and observed no effect on gut community structure, even though the relative abundance of Rhodobacterales in the GI tract decreased.
Pseudoalteromonas
Gauthier et al. (1995) proposed that genus Pseudoalteromonas, aerobic, non-spore forming rods was split from Alteromonas. They produce a broad range of anti-bacterial products (Jin et al., 2010; Offret et al., 2016; Richards et al., 2017), and are reported in finfish intestine (e.g., Fjellheim et al., 2007; Ringø et al., 2008; Jiang et al., 2018), as probiotics (Mladineo et al., 2016), and as a part of a multi-strain probiotic preparations with Microbacterium, Ruegeria and Vibrio fed to Atlantic cod larvae (Skjermo et al., 2015).
In a study using Pseudoalteromonas sp. Administrated to European sea bass (Dicentrarchus labrax), Mladineo et al. (2016) documented best stimulation of phagocytic activity, respiratory burst, and gene expression of lysozyme, Mx protein, caspase 3, TNF-a, and IL-10, by Pseudoalteromonas compared to Alteromonas sp. And Enterovibrio coralii administration.
Pseudomonas
Genus Pseudomonas belong to family Pseudomonadaceae, are rod-shaped, aerobic, catalase- and oxidase positive and contain approximately 200 species. The genus has a great metabolic diversity (Palleroni, 1992; Silby et al., 2011), and produce exopolysaccharides, which could make it difficult for pseudomonads to be phagocytosed by mammalian white blood cells and contribute to surface-colonizing biofilms that are difficult to remove from food preparation surfaces (Royan et al., 1999).
Several studies have revealed the probiotic potential of Pseudomonas (e.g., Giri et al., 2011; Giri et al., 2015; Giri et al., 2016), and they are able to colonize a wide range of niches, including the GI tract of finfish (e.g., Ringø et al., 1997; Ringø et al., 2006a; Navarrete et al., 2013; Wang et al., 2020a).
Genus Pseudomonas is frequently used in finfish aquaculture, and in order to avoid overlaps, previous studies discussed in the review of De et al. (2014); Hayatgheib et al. (2020) and Irianto and Austin (2002a) are only briefly presented in Table 1. Siderophore-producing Pseudomonads strains have successfully been applied as biocontrol agens to finfish. In an early study, Smith and Davey (1993) showed that the fluorescent pseudomonad F19/3 isolated from Atlantic salmonatlantic salmon (Salmo salar) with furunculosis inhibitied in vitro growth of A. salmonicida in culture media, and improved resistance of presmolts of brown trout (Salmo trutta) against A. salmonicida and the authors suggested that this finding was due to that the strain inhibited the pathogen by competing for free iron. Similarly, Pseudomonas fuorecens was regarded as effective probiont for rainbow trout conferring protection against V. anguillarum (Gram et al., 1999), but the strain did not protect Atlantic salmon against A. salmonicida despite that in vitro inhibition was revealed (Gram et al., 2001). (Korkea-aho et al. (2012) revealed that Pseudomonas sp. M162 administrated to rainbow trout fry colonised the GI tract, improved immunity and protection against F. psychrophilum, while administration of P. fluorescens at a inclusion level of 107 displayed enhanced growth rate, and feed conversion ratio of African catfish (Clarias gariepinus) (Osungbemiro et al., 2018). Haematological analyses of African catfish fed the P. fluorescens diets had significantly higher white blood cell than control diet. In addition, lower mortality rate and several intestine histopathological alterations were revealed in catfish fed diets supplemented with P. fluorescens. In two recent studies, González-Palacios et al. (2019; 2020) revealed that two P. fluorescens isolated from skin of trout could adhere to mucus, reduced adhesion of zoospores and cysts of S. paracitica in rainbow trout, stimulated phagocytic activity of macrophages, serum lysozyme activity and serum protein concentration, and might be promising for biocontrol of saprolegninosis. Giri et al. (2020) conducted a 8 weeks feeding trial with juvenile common carp to determine the effect of heat-killed Pseudomonas aeruginosa strain VSG2, and revealed enhanced lysozyme, protein level, and alkaline phosphatase. In serum and skin mucus, superoxide dismutase, glutathione, glutathione peroxidase, and myeloperoxidase levels significantly enhanced. Furthermore, mRNA expression of antioxidant genes significantly improved in liver. These positive effects were also noticed by improved resistance against A. hydrophila. Qi et al. (2020) displayed that Pseudomonas monteilii JK-1 significantly inhibited in vitro growth of A. hydrophila, and based on this criterion administrated the bacteria to grass carp, and showed that the bacteria was not toxic to the fish, and improved resistance against A. hydrophila. According to Fu et al. (2017), administration of Pseudomonas stutzeri F11 to grass carp reduced the levels of ammonia-N, nitrite-N, and total N in the water over an extended range, but administration did not had any effect on nitrate-N level. Modulation of the water microbial community was observed, by increasing the relative abundance of Bacteroidetes and Firmicutes, in contrast to Proteobacteria, Actinobacteria and Verrucomicrobia which decreased.
P. aeruginosa strain VSG2 has also been used in a multi-strain probiotic preparation with Bacillus subtilis and Lactobacillus plantarum (Giri et al., 2015), revealing improved growth performance, immunity and disease resistance in rohu.
Psychrobacter
Genus Psychrobacter belongs to the family Moraxellaceae, are Gram-negative aerobic, oxidase-negative, catalase-positive, non-pigmented and non-motile coccoid bacteria. Information is available showing the presence of Psychrobacter in intestine of finfish (e.g., Bakke-McKellep et al., 2007; Ringø et al., 2006a; Ringø et al., 2016b), and some Psychrobacter strains have successfully been used as probiotics to finfish (Sun et al., 2011; Sun et al., 2014; Makled et al., 2017; Makled et al., 2020).
Sun et al. (2011) administrated Psychrobacter sp. SE6 to grouper (Epinephelus coioides) and revealed only improvement in feed conversion ratio and serum component 4, while no effect was noticed on weight gain, specific growth rate (SGR), hepatopancreatic protease and lipase activity, intestinal amylase activity, and serum lysozyme - and superoxide dismutase activity, and serum component 3. In a later study, Sun et al. (2014) revealed that viable SE6 administration upregulated expression of TRL2 and TRL5 and cytokines, while results of heat-inactivated SE6 administration revealed that the MyD88-independent TLR2 signaling pathway was involved in the recognition of SE6. Use of Psychrobacter namhaensis administrated to Nile tilapia for 50 days, showed improved growth rate and feed utilisation ratio, haematocrit-, haemoglobin-, erythrocytes- and total leucocytes values by 2.8 x 107 CFU mL-1 supplementation vs. control fish (Makled et al., 2017). Moreover, immunoglobulin, alternative hemolysis, phagocytic and lysozyme activities significantly increased by feeding similar administration level. In a later study by the same authors, Makled et al. (2020) used Psychrobacter maritimus S, isolated from sediment as probiont to Nile tilapia. Growth rates, digestive enzymes (protease, lipase and amylase), phagocytic- and lysozyme activity, alternative complement hemolysis, hematological parameters significantly increased by 3.3 x 108 CFU mL-1 feeding, but slightly decreased at the highest inclusion level. Similarly, expression of interleukin-4 and 12 genes was significantly up-regulated by 3.3 x 108 CFU mL-1 feeding, while heat shock protein gene was down-regulated. Based on their results, the authors concluded that P. maritimus S at inclusion level of 3.3 x 108 CFU mL-1 is a promising probiont for Nile tilapia fingerlings.
Even though some information is available on Psychrobacter as probiotic in finfish, the genus deserves more attention as findings indicate that Psychrobacter might be capable of producing and secrete antimicrobial compounds (Wanka et al., 2018).
Rhodopseudomonas palustris
Rhodopseudomonas palustris is a rod-shaped photosynthetic bacterium, with an ability to switch between four different modes of metabolism. The bacterium has been isolated from swine waste lagoons, earthworm droppings, marine coastal sediments, sludge for use in a recirculating aquaculture system (Kim et al., 1999), pond water (Wang, 2011; Zhang et al., 2014), used in fluidizes bed biofilters (Zhan and Liu, 2013), and in some probiotic studies (Zhou et al., 2010; Wang, 2011; Zhang et al., 2014; Liu et al., 2020).
Zhou et al. (2010) revealed that administration during 40 days of a diet supplemented with R. palustris GO6 increased significantly the tilapia growth performance, respiratory burst-, superoxide dismutase-, catalase- and myeloperoxidase activities, while no effect was revealed regarding total serum protein, albumin, globulin, serum lysozyme content. In this study, administration of two bacilli species were included, and the author’s conclusion was Bacillus coagulans, followed by G06 were better water additives than B. subtilis to tilapia. In a 60-day study with grass carp, Wang (2011) reported that R. palustris administration enhanced growth performance and amylase activity in proximal intestine (PI) and distal intestine (DI), while protease- and cellulase activities in PI and DI were not affected. Although R. palustris supplementation revealed some positive effect, the best results were revealed by Bacillus coagulans. Zhang et al. (2014) demonstrated that R. palustris administration to grass carp culture significantly decreased ammonia-N, total inorganic-N and total-N in water, and modulated the water microbiota, by affecting the relative abundance of Proteobacteria, Bacteroides and Actinobacteria. In a study with yellow catfish (Pelteobagrus vachelli), Liu et al. (2020) revealed that R. palustris in effluent increased protease-, amylase-, and lipase activities, and alkaline phosphatase, acid phosphatase, superoxide dismutase and catalase by up-regulating gene expression. Furthermore, disease resistance towards A. hydrophila, and modulation of the gut microbiota was observed by significantly increased the relative abundance of bifidobacteria and lactobacilli.
Roseobacter
Roseobacter species have been identified as both oval and rod-like shaped motile cells, are marine species and have a major role in oceanic sulfur cycling (Buchan and Moran, 2005; Wagner-Döbler and Biebl, 2006). They are heterotrophs, anaerobic and possess N-acyl homoserine lactones (AHLs) based quorum sensing systems (Tang et al., 2010; Cude and Buchan, 2013). During the last years, information has become available showing the presence of Roseobacter in intestine of finfish (e.g., Hjelm et al., 2004; Fjellheim et al., 2007).
Roseobacter species as candidate probiotic bacteria of the fish could antagonize fish-pathogenic bacteria without harming the fish or their live feed. Makridis et al. (2005; 2008) revealed similar survival of gilthead sea bream larvae exposed to 6 x 105 Roseobacter mL-1 when larvae were reared in sterile seawater, while lower survival was noticed when larvae were held in filtered seawater. spp. sp.
Roseobacter species revealing antagonism against Vibrio species in combination with algae could be a possible probiotic organism in larval rearing.
Shewanella
The genus is included in family Shewanellaceae, is facultative anaerobic in the absence of oxygen, and members of the genus have capabilities to use of a variety of electron acceptors for respiration. Most of the bacteria in the genus are revealed in extreme aquatic habitats, at low temperature, and at high pressure. Shewanella are a normal component of the surface microbiota of several finfish species (e.g., Satomi et al., 2006; Fjellheim et al., 2007; Satomi et al., 2007; Navarrete et al., 2013; Egerton et al., 2018).
Genus Shewanella is one of the most frequently used Gram-negative probiotics in finfish aquaculture, as the bacterium inhibit in vitro growth of Photobacterium damselae subsp. piscicida, Vibrio harveyi, Vibrio alginolyticus and V. anguillarum (Chabrillón et al., 2005a; Chabrillón et al., 2005b; Chabrillón et al., 2006).
Within genus Shewanella, is Shewanella putrefaciens Pdp11 most frequently used. Guzmán-Villanueva et al. (2014) used Pdp11 as a probiotic supplementation to gilthead seabream (14.5 g) in a 4-week study, and revealed significant lower serum IgM levels, and serum peroxidase activity after 4 weeks, while growth performance (SGR and condition factor), serum antiprotease -, leucocyte peroxidase- serum antiprotease and leucocyte peroxidase activities were unaffected by probiotic feeding compared to control fed fish. In two studies using enriched of Artemia by S. putrefaciens Pdp11 to Senegalese sole (Solea senegalensis) larvae, Lobo et al. (2014a; 2014b), revealed improved growth and modulation of the gut microbiota. In a later study, Lobo et al. (2016) showed that Artemia metanauplii used as live vector for Pdp11 administration, improved growth of the sole and affected lipid profile.
In a recent study, Chen et al. (2020b) revealed that administration of Pdp11 facilitated wound closure, and increased the albumin/globulin ratio, protease and peroxidase activities in skin mucus, 7 days after post-wounding, but decreased serum aspartate aminotransferase. In addition, probiotic administration up-regulated gene expression of antioxidant enzymes and anti-inflammatory cytokines (il-10 and tgf- β) but decreases pro-inflammatory cytokines (il-1 β, il-6, il-8 and tnf-α). Based on their results, the authors concluded that Pdp11 had a positive effect on wound healing and skin damage. This conclusion was strengthened by Chen et al. (2020c) evaluating administration of Pdp11 on gene expression of the intestinal inflammatory response and barrier function of gilthead seabream.
An interesting approach regarding probiotics, using Shewanella sp. MR-7 isolated from turbot intestine that could utilize soybean meal (SBM) in turbot intestine was evaluated by Li et al. (2019b). SBM fermented by the bacterium and fed to turbot counteracted inflammatory response and modulated mucosal microbiota at both phylum and genus level, but no significant effect was noticed on trypsin, diastase (catalyze the breakdown of starch into maltose) and lipase activities. These interesting findings merit further investigations by including disease-, immunological- and gene expression studies.
S. putrefaciens Pdp11 is also used in combination with Bacillus sp. and palm fruits extracts in a study evaluated antioxidant enzyme gene expression in the mucus of gilthead seabream (Sparus aurata L.) (Esteban et al., 2014).
According to Seoane et al. (2019), S. putrefaciens Pdp11, presents features that can explain its probiotic benefits; specific proteins for adhesion and colonization of the GI tract, resistance to bile salt, and inhibition of pathogen adhesion in the gut.
A dietary supplementation of Shewanella xiamenensis A-1 and A-2 isolated from grass carp was administrated to grass carp for 28 days and thereafter challenged with A. hydrophila (Wu et al., 2015). A significant enhancement of respiratory burst, and phagocytic and lysozyme activities, and upregulation of immune related genes (IL-8, IL-1β, lysozyme-C and TNF-α), and resistance against A. hydrophila were revealed. In later study, Hao et al. (2017) supplemented grass carp diet with a dose of 108 CFU g−1 of S. xiamenensis for 28 days, and at the end of feeding modulation of the gut microbiota was noticed. The relative abundance of Meganema and Rubellimicrobium increased, Lactococcus, Pseudomonas and Citrobacter (cellulose degrading bacteria) decreased, while Flavobacterium was not detected compared to control fed fish.
Asaduzzaman et al. (2018) revealed that administration of Shewanella sp. to Malaysian Mahseer for 90 days, improved gut histology (villi height, villi with and villi area), gut production of SCFAs, and modulated the gut microbiota. In a more recent study, administration of Shewanella sp. MR-7 to turbot, ameliorate lipopolysaccharide induced intestinal dysfunction (villus and microvilli height), and modulated the gut microbiota by enhancing the relative abundance of Lactobacillus, and reducing the relative abundance of Pseudomonas (Zhang et al., 2020).
Aliivibrio
The taxonomy and phylogeny of genus Photobacterium is revised, for example, Photobacterium logei and Photobacterium fischeri are now considered members of genus Aliivibrio (Labella et al., 2017). Aliivibrio is reported in the intestinal tracts of vertebrates as well as finfish (Green et al., 2013; Karlsen et al., 2017; Rud et al., 2017; Hamilton et al., 2019), and some information is available on their use as probiotics in finfish aquaculture.
Vibrio viscosus reclassified as Moritella viscosa (Benediktsdottir et al., 2000) is a bacteria species associated with “winter ulcer”, affecting salmonids reared in seawater. In two recent studies, Klakegg et al. (2020a; 2020b) investigated the effect of Aliivibrio strains isolated from the mandibulum of farmed Atlantic salmon on growth performance and ulcer prevalence of Atlantic salmon, and ulcer prevalence of lumpfish (Cyclopterus lumpus), respectively. Both studies, revealed improved growth performance and ulcer prevalence after adding Aliivibrio into the tank water. Based on their results, the author suggested that Aliivibrio administration may have impact on welfare, economy and sustainability in aquaculture as fewer ulcer outbreak caused by M. viscosa was noticed.
Enterovibrio
In a study evaluating Enterovibrio coralii administration to European sea bass (Dicentrarchus labrax), Mladineo et al. (2016) revealed no significant stimulation of phagocytic activity, respiratory burst, and gene expression of lysozyme, Mx protein, caspase 3, TNF-a, and IL-10.
Vibrio
Genus Vibrio has a curved-rod (comma) shape, are reported in salt water, and are facultative anaerobe and oxidase positive bacteria. Even through several species of Vibrio are among the most common bacteria leading to massive mortality of cultured fish, and shellfish (Ina-Salwany et al., 2019), several studies have reported that Vibrio is dominant in the GI tract of fish (e.g., Eddy and Jones, 2002; Fonseca et al., 2019). Even though genus Vibrio are pathogenic, several studies have used apathogenic Vibrio as probiotic in finfish aquaculture (Austin et al., 1995; Gatesoupe, 1997; Ringø and Vadstein, 1998; DeSchrijver and Ollevier, 2000; Ottesen and Olafsen, 2000; Makridis et al., 2001; Aerts et al., 2018; Schaeck et al., 2016), as well as a part in a multi-strain probiotic supplementation with Microbacterium, Ruegeria and Pseudoalteromonas (Skjermo et al., 2015), and in combination with A. veronii and Flavobacterium sasangense (Chi et al., 2014).
In an early study, Ottesen and Olafsen (2000) evaluated the effect of water administration of Vibrio iliopiscarius and apathogenic Vibrio salmonicida on Atlantic halibut (Hippoglossus hippoglossus) larval survival. Pre-incubation of larvae with apathogenic V. salmonicida improved survival to 94.4%, whereas V. iliopiscarius administration reduced survival to 63% compared to 81% survival in the control group.
Makridis et al. (2001) reported the use of Vibrio strain PB 1-11 and strain PB 6-1 encapsulated in Artemia franciscana and revealed that total CFU in water was lower by encapsulation, while larval gut microbiota was not significantly affected by encapsulation. Schaeck et al. (2016) used a Vibrio lentus as probiotic supplement in a study with gnotobiotic European sea bass (Dicentrarchus labrax) larvae, and displayed improved resistance against V. harveyi, but administration of Vibrio proteolyticus did not revealed any effect on larval survival. In a following study, Schaeck et al. (2017) revealed that V. lentus administration to gnotobiotic European sea bass larvae significantly modified gene expression did not affect apoptotic and cell proliferative indexes. Aerts et al. (2018) evaluate the probiotic potential of V. lentus, as inoculum into well water containing gnotobiotic European sea bass larvae at day 8 post hatching, and revealed significantly decreased glucocorticoid baseline levels in larvae, and the authors suggested that their findings provided a better insight into the hypothalamic-pituitary-interrenal axis. Furthermore, Vibrio species, such as Vibrio natriegens which show high capacity to hydrolyze casein, could increase feed efficiency and improve the growth rate of fish (Rahman et al., 2016).
Gram-Positives
The beneficial effects of Gram-positive probiotic bacteria used in finfish aquaculture, and studies discussed in the review of De et al. (2014); Hayatgheib et al. (2020); Tran et al. (2020) and van Doan et al. (2021) are only briefly presented in Table 2.
Table 2 Effect of Gram-positive bacteria on growth performance, gut health, immune system and disease resistance in finfish, and an in vitro study.
Arthrobacter
Genus Arthrobacter, has no spores and capsule, utilizes a wide and diverse range of organic substances, and has ability to produce antimicrobial compounds (O’Brien et al., 2004; Papaleo et al., 2012). They are reported in finfish intestine (e.g., Ringø et al., 2006a; Ringø et al., 2008; Nayak, 2010; Wang et al., 2019b), but less information is available on their use as probiotic to finfish (Lauzon et al., 2010). Some information is available on its use in a multi-strain probiotic mixture (Geng et al., 2012a; Peixoto et al., 2018).
An Arthrobacter sp. strain that showed inhibitory potential against fish pathogens in vitro was used in a bath treatment of Atlantic cod larvae (Lauzon et al., 2010), and regularly administration to the rearing water, revealed that the bacterium could establish in the larval intestine.
Bifidobacterium
Numerous health benefits have been claimed for genus Bifidobacterium, the “good bacteria”. Compared to Lactobacillus acidophilus, are bifidobacteria less acid tolerant as they do not grow below pH 5.0 (Shah, 1997), while Lb. acidophilus grow below 4.0. Bifidobacterium are reported in the GI tract of finfish (Vlkova et al., 2012; Piazzon et al., 2019; Wang et al., 2020b), but Bifidobacterium is less incorporated into diets or added to the rearing water in finfish aquaculture (Sahandi et al., 2017; Sahandi et al., 2019). In addition, Bifidobacterium bifidium was administrated to Siberian sturgeon (Acipenser baerii) in combination with Lactobacillus spp. and B. subtilis, and the results revealed improved growth performance, hematological and immune parameters (Hassani et al., 2020).
In two studies with rainbow trout, Sahandi et al. (2017; 2019) used two bifidobacteria, Bifidobacterium animalis PTCC-1631 and Bifidobacterium animalis subsp. lactis PTCC-1736, isolated from rat feces and fermented milk, respectively, and administration of 107 CFU g-1, revealed positive effect on growth, nutrient utilization, digestibility, feed conversion ratio, red and white blood cell content, serum biochemical and reduction of cortisol level of rainbow trout.
in vitro Brochothrix
Genus Brochothrix is non-spore-forming, non-motile catalase-positive, facultative anaerobic, rod-shaped bacteria that show characteristic changes in cell morphology during growth. Sneath and Jones (1976) proposed the genus for some meat spoilage bacteria, previously designated as Microbacterium thermosphactum. The scientific interests have mostly focused on Brochothrix thermosphacta as the bacterium is associated with off-odour development in meats, especially in prepacked products held at refrigeration temperatures. They are isolated from the GI tract of finfish (Ringø et al., 2006a; Ringø et al., 2008; Higuera-Llanten et al., 2018), but less information is available on their use as probiotics in aquaculture (Pieters et al., 2008).
Administration of B. thermosphacta BA211 at 1010 g-1 in rainbow trout diet for 2 weeks increased fish survival against challenge with Aeromonas bestiarum (Pieters et al., 2008).
Clostridium
Genus Clostridium is a butyric‐acid producer, and butyrate is the preferred energy source for the colon epithelial cells, contributes to the maintenance of the gut barrier functions, and has immunomodulatory and anti-inflammatory properties (Riviere et al., 2016; Guo et al., 2020). Clostridium are isolated from finfish intestine (e.g., Wu et al., 2012; Abdelhamed et al., 2019; Pérez-Pascual et al., 2020; Rimoldi et al., 2020), and some strains are frequently used as probiotics to enhance growth and immune response in finfish (for review see Tran et al., 2020; Table 2) as well as in shellfish aquaculture (Ringø, 2020; Tran et al., 2020).
Single cell protein of Clostridium autoethanogenum has been evaluated in four recent studies (Table 2). Chen et al. (2019a) evaluated the effect of partial replacement of fish meal with C. autoethanogenum single-cell protein (CAP) fed to juvenile black sea bream (Acanthopagrus schlegelli) and revealed that dietary treatments did not significantly affect malondialdehyde, catalase, total antioxidant capacity and digestive protease, lipase and amylase activities. On the other hand, total superoxide dismutase in serum of fish fed the highest inclusion CAP level, 58.2%, was significantly lower than that of control fed fish.
An overview on the use of C. butyricum as probiotics was presented by Tran et al. (2020) and to avoid overlaps, the results discussed in the abovementioned review are only summarized in Table 2. He et al. (2017) noted no effect on growth performance, digestive enzyme activities, serum- lysozyme, catalase and glutathione peroxidase activities, but only improved serum superoxide activity by feeding hybrid grouper (Epinephelus lanceolatus ♂ x Epinephelus fuscoguttatus ♀) C. butyricum, at inclusion level of 109 CFU kg-1, compared to fish fed only Lb. acidophilus or a combination with Lb. acidophilus, Bacillus cereus and C. butyricum. In a recent study, Meng et al. (2021) administrated a commercial C. butyricum at two inclusion levels; 0.25 x 107 (LVB) and 107 (HCB) CFU g−1, for 8 weeks to address the effect on intestinal enzyme activity, SCFAs, intestinal gene expression and diversity of intestinal microbiota of common carp (Cyprinus carpio). A substantial beneficial effect was noticed, probiotic administration by HCB significantly enhanced intestinal catalase and lysozyme, positively affected mucin secretion and the height of microvilli, and intestinal gene expression of IL-10, TLR-2, MyD-88, ZO-1 and Occludin. Butyric- and propionic acid content were elevated in both clostridia treatments. Furthermore, the intestinal content microbiota was affected, with improved abundance of Bacteroides and a significant decrease in Fusobacteria and Proteobacteria. Zhang et al. (2020) used a commercial C. butyricum strain, previously used in shellfish studies at three administration levels. The authors revealed that inclusion level of 1.5x1011 CFU kg-1, improved growth performance, digestive enzymes (amylase, lipase and trypsin), and antioxidant capacity in spleen, head kidney and liver of tilapia. Furthermore, modulation of the gut microbiota, functions related to phosphorylation, proteinases, and nitrogen metabolism were noticed.
Kocuria
Kocuria was first reported by Kocuria is coccus shaped, and have rigid cell walls and are either aerobic or facultative anaerobic bacteria (Venkataramana et al., 2016), and has been isolated from the GI tract of finfish (e.g., Bakke-McKellep et al., 2007; Linh et al., 2018; Sharifuzzaman et al., 2018).
According to Vine (2004) Kocuria AP4 administrated to clownfish larvae, improved survival. Rainbow trout orally fed Kocuria SM1 (108 cells g-1) originally isolated from GI tract of rainbow trout, has been administrated to rainbow trout in three studies (Sharifuzzaman and Austin, 2010a; Sharifuzzaman and Austin, 2010b; Sharifuzzaman et al., 2011). In a later study using Kocuria SM1, Sharifuzzaman et al. (2014) revealed increase in in epidermal mucus and goblet cells in hindgut, but growth performance, gut histology in pyloric caeca and foregut, serum biochemical parameters (hemoglobin, urea, creatinine and glucose), and digestive enzymes activity (API ZYM test) were not affected by probiotic feeding, while a notable decrease in vacuole-containing enterocytes was noticed. Furthermore, an interesting finding was that inflammation was not observed in fish fed Kocuria SM1. In most probiotic studies, the frequency of the probiont is evaluated after continuous feeding, but in the study of Sharifuzzaman et al. (2014) probiotic feeding by Kocuria SM1or Rhodococcus SM2 was stopped after 14 days and reverted back to the control diet for 14 days. The results of both probiotic bacteria revealed that percentage of the probiont in digesta reached maximum, at the end of day 14, but disappear upon switching to the control diet after 28 days. The authors concluded that this observation indicate no primary colonization in the GI tract, but to fully conclude the autochthonous microbiota should be analyzed.
Microbacterium
Genus Microbacterium belongs to the family Microbacteriaceae within suborder Micrococcineae. Microbacterium are non-spore-forming, rod-shaped bacteria, and was classified according to the amended genus description by Collins et al. (1983) and redefinition of Takeuchi and Hatano (1998). They are isolated from the GI tract of finfish (e.g., Ringø et al., 2006a; Ringø et al., 2006b; Hu et al., 2015), used as probiotics (Fjellheim et al. (2010), and in a multi-strain probiotic mixture with Pseudoalteromonas, Ruegeria and Vibrio fed to Atlantic cod larvae (Skjermo et al., 2015).
In a study to evaluate the selection of candidate probiotics, Fjellheim et al. (2010) revealed that Microbacterium sp. ID-3-10 improved survival of Atlantic cod larvae exposed to V. anguillarum 02a.
Micrococcus
Genus Micrococcus was divided into Micrococcus, Kocuria, Nesterenkonia, Kytococcus and Dermacoccus based on phylogenetic and chemotaxonomic studies by Stackebrandt et al. (1995). Information is available on their presence in finfish intestine (e.g., Ringø, 1993; Bakke-McKellep et al., 2007; Hu et al., 2015), and furthermore information is available on the potential of gut Micrococcus isolates as probiotics (e.g., Nurhidayu et al., 2012; Akayli and Urku, 2014; Akayli et al., 2016), and their use as probiotics in finfish aquaculture (Irianto and Austin, 2002b; Abd El-Rhman et al., 2009; Sankar et al., 2017).
Feeding Micrococcus luteus to rainbow trout and Nile tilapia, reduced mortality after challenged with A. salmonicida (Irianto and Austin, 2002b) and A. hydrophila Abd El-Rhman et al. (2009). In a later study, Sankar et al. (2017) evaluated the effect of Micrococcus administration on digestive enzymes (pepsin, α-amylase, protease and lipase) activities, and revealed differences in pearl spot (Etroplus suratensis) and tilapia after 60 days feeding.
Paenibacillus
Previously, Paenibacillus species were included in genus Bacillus due to their common morphological and physiological characteristics. However, based on 16S rRNA gene sequences in 1993, Paenibacillus was reassigned as a new genus. Genus Paenibacillus has been isolated from humans, animals, plants as well as fish (Midhun et al., 2017; Ma et al., 2018; Wang et al., 2019c), but their use as probiotics in finfish aquaculture is less investigated.
Common carp fry administrated with Paenibacillus polymyxa improved growth performance, non-specific immune (lysozyme, respiratory burst and myeloperoxidase activities), and resistance against A. hydrophila (Gupta et al., 2014). Later the same authors (Gupta et al., 2016) revealed that P. polymyxa supplemented to the water at three concentrations, improved water quality, common carp survival, innate immune response (lysozyme, respiratory burst, myeloperoxidase, catalase and superoxide dismutase activities), and resistance against A. hydrophila, at 103 and 104 CFU mL-1 supplementation. In a recent study, Chen et al. (2019b) demonstrated that administration of Paenibacillus ehimensis enhanced growth performance, immune parameters, and resistance against A. hydrophila and S. iniae.
Rhodococcus
Genus Rhodococcus is aerobic, nonsporulating, non-motile bacteria closely related to Mycobacterium and Corynebacterium. Few species are pathogenic and Rhodococcus have been revealed in a broad range of environments, including soil and water, as well as fish intestine (Tapia-Paniagua et al., 2014a; Song et al., 2016; Sharifuzzaman et al., 2018). Strains of Rhodococcus is experimentally advantageous due to its relatively fast growth rate and simple developmental cycle.
In a study by Sharifuzzaman et al. (2011), the authors used paraprobiotic (cellular components) of Rhodococcus SM2 isolated from the intestine of rainbow trout and displayed enhanced trout immune response and a significant resistance to V. anguillarum challenge. In a subsequent study, Sharifuzzaman et al. (2014) revealed that administration with Rhodococcus SM2, ~ 107 CFU g-1 for 14 days, epidermal mucus and goblet cells in hindgut increased, while no significant effect was noticed on growth performance, gut histology in pyloric caeca and foregut, digestive enzymes activity, and serum biochemical parameters. Inflammation was not observed in fish fed Rhodococcus SM2.
In a study with brook charr (Salvelinus fontinalis), Rhodococcus sp. originally isolated from skin mucus of brook charr and added to the tank water twice a day at a concentration of 105 mL−1, Boutin et al. (2013) observed that the bacteria did not colonize the skin mucus, but was detected in the biofilm of the tank. An interesting beneficial effect was noticed, the population of the pathogen F. psychrophilum decreased in water by modulating the water microbiota. Furthermore, the bacterial communities in water samples were more diverse than the skin mucus microbiota.
An interesting aspect of Rhodococcus was recently evaluated by Garai et al. (2021), as they investigated degradation of mycotoxin. This is highly relevant as mycotoxins are secondary metabolites of fungi, which are common in food, and from time to time also present in aquafeed (Pietsch, 2020).
Multi-Strain Probiotics
In aquaculture, multi-strain probiotics have been considered to be more effective than a single strain in aquaculture, and readers with special interest in this topic, are referred to the recent reviews of Melo-Bolivar et al. (2021).
Conclusions and Further Directions
Nearly 90% of the global aquaculture production is carried out in countries in Asia, and the development is so fast that infectious disease outbreak happens regularly, and to solve this problem antibiotics are used with few regulations. However, the abuse of antibiotic treatment in aquaculture with tetracycline, β-lactams, sulfonamides, quinolones etc. results in development of antibiotic resistance in the pathogens, accumulation of residual in finfish products, depression of immune system, and translation of resistant genes to terrestrial animals and humans. Therefore action for alternative treatment methods in aquaculture are needed. In addition to the concept of probiotics, paraprobiotic is relatively established in higher vertebrate models and related food production sectors, but its application in aquaculture is still in its early stage (Choudhury and Kamilya, 2019; Teame et al., 2020), and merits investigations. Another alternative method is postbiotic that may be useful in aquaculture (Ang et al., 2020; Cuevas-González et al., 2020; Teame et al., 2020), a topic that merits further studies.
Moreover, peptides and exopolysaccharides revealed antimicrobial properties against bacterial pathogens, and SCFAs display both antimicrobial activities against bacterial pathogens and immune stimulating effects to aquatic organism, and cell surface proteins and teichoic acid can act as vaccine. Furthermore, it is well known that dietary manipulation affect the gut microbiota and improve fish health (e.g., Ringø et al., 2016; Turchini et al., 2022).
Dose as defined as the concentration (number of probiotic cells) must be carefully determined, as overdosing may result in lower efficacy with increasing costs, and under dosing could reduce the efficacy of the probiont. Previously, administration doses between 104 and 106 cells mL-1 to the total culture volume was suggested to be sufficient in introducing a probiotic capable of dominating the intestinal microbiota (Vine et al., 2006), but nowadays doses between 107 and 109 cells mL-1 are used. However, in order to maintain the desired probiotic concentration in the culture water, additional doses may be required, and its frequency may depend on the probiotic species, stage of fish development, diet, culture conditions (Verschuere et al., 2000).
Even though focus has been directed towards LAB and bacilli within probiotics in aquaculture (e.g., Ringø et al., 2018; Ringø et al., 2020a; James et al., 2021; Nayak, 2021), we strongly recommend the scientific community to focus on other interesting probionts. They play important roles in mediating and stimulating GI development, aiding digestive function, maintaining mucosal tolerance, enhance the immune response, and provide protection against diseases, development of metabolic syndrome, vitamin synthesis, modulation of the gut microbiota, and interactions on the gut-brain axis and gut-kidney axis. In addition, multistrain probiotic administration increased the gut microbiota diversity (Halkjær et al., 2020) illustrating that the gut microbiota merits further investigation in finfish aquaculture.
Probiotic applications may be extended in aquaculture with the use of exo-enzymes producing strains in bioprocessing of the complex feed ingredients and diverse microbial bio-active compounds and/or metabolites (e.g., antimicrobial compounds, quorum quenching enzymes, SCFA as functional feed additives. Along with probiotic potential, studies should be directed to develop the probiotic-products as synbiotics or postbiotics and their efficacy in culture condition are required to be evaluated.
The beneficial effects of LAB and Bacillus and their bacteriocins as alternatives to antibiotic growth promoters in animal production is well known (e.g., Caulier et al., 2019; Vieco-Saiz et al., 2019). However, as no information is available on bacteriocins from other promising probiotics in aquaculture, we highly recommend that this topic receive more attention.
Bacteria communicate with one another using chemical signal molecules, a process, and termed quorum sensing (QS), the enzymatic degradation of AHLs, has been suggested as a promising strategy to control bacterial diseases (e.g., Defoirdt, 2018; Ghanei-Motlagh et al., 2020). For example, Ghanei-Motlagh et al. (2020) revealed that Shewanella isolated from Asian sea bass showed high ability to degrade synthetic- and natural AHLs produced by V. harveyi and V. alginolyticus.
Within the probiotic bacteria discussed in the present study, a topic that merits investigation is the interactions between probiotics and antioxidant properties, a topic reviewed by Wang et al. (2017).
Even though probiotic inclusion in the diet is the most frequently used administration method, several studies have administrated probiotics in the water (Jahangiri and Esteban, 2018; the present study). However, to fully conclude that water administration is a suitable method, further studies need to be conducted in intensive production.
In the conclusion, application of beneficial microbes is a sustainable approach.
Author Contributions
ER: Introduction, Acinetobacter, Alcaligenes, Aliivibrio, Arthrobacter, Bifidobacterium, Brochothrix, Chromobacterium, Clostridium, Enterovibrio, Kocuria, Microbacterium, Micrococcus, Paenibacillus, Phaeobacter, Pseudoalteromonas, Rhodococcus, Rhodopseudomonas, Shewanella and editorial. XL: Pseudomonas, Roseobacter, Vibrio and Rhodosporidium. HD: Aeromonas, and Alteromonas. KG: proofreading, editing and provided critical feedback in revision. All authors contributed to the article and approved the submitted version.
Funding
The publication charges for this article have been funded by a grant from the publication fund of UiT The Arctic University of Norway.
Conflict of Interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher’s Note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
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Keywords: probiotic bacteria, non-LAB, bacilli, finfish, aquaculture
Citation: Ringø E, Li X, Doan Hv and Ghosh K (2022) Interesting Probiotic Bacteria Other Than the More Widely Used Lactic Acid Bacteria and Bacilli in Finfish. Front. Mar. Sci. 9:848037. doi: 10.3389/fmars.2022.848037
Received: 03 January 2022; Accepted: 29 April 2022;
Published: 02 June 2022.
Edited by:
Benjamin Costas, University of Porto, PortugalReviewed by:
Ana Teresa Gonçalves, GreenCoLAB, PortugalFrancisco Vargas-Albores, Consejo Nacional de Ciencia y Tecnología (CONACYT), Mexico
Viswanath Kiron, Nord University, Norway
Copyright © 2022 Ringø, Li, Doan and Ghosh. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Einar Ringø, RWluYXIuUmluZ29AdWl0Lm5v; orcid.org/0000-0002-4940-5688