Editorial: Dealing with unusual hosts and unconventional habitats: versatile strategies of Salmonella enterica

Editorial on the Research Topic
Dealing with unusual hosts and unconventional habitats: versatile strategies of Salmonella enterica

Salmonella enterica, a member of the Enterobacteriaceae family, may cause gastroenteritis, typhoid fever, and systemic infections in a wide range of hosts, including humans, animals, and birds. Recent investigations revealed that S. enterica is a highly adaptable bacterium, capable of colonizing and persisting in unconventional habitats and hosts. This notion challenges the traditional understanding of S. enterica ecology and classical host-pathogen interaction studies.

A remarkable feature of S. enterica is its ability to adapt to diverse ecological niches. While this bacterium has long been associated with human and animal diseases, many studies have identified non-traditional hosts, such as plants, protozoa, and insects, as reservoirs for S. enterica. Understanding the mechanisms behind the adaptation to such a broad host range is crucial for comprehending the epidemiology and transmission dynamics of Salmonella-associated diseases. Salmonella has been found in water sources, soil, and even within biofilms on plastic surfaces. This versatility raises concerns regarding traditional sanitation and hygiene practices since S. enterica presence complicates efforts to prevent infections. Exploring the molecular mechanisms that allow S. enterica to persist in unusual environments is essential for developing effective strategies to mitigate contamination.

Salmonella enterica employs an array of survival strategies to thrive in unconventional hosts and habitats. These strategies include biofilm formation, stress response mechanisms, alternative metabolic pathways and the ability to change its phenotype. Biofilm formation enables Salmonella to adhere to surfaces, while stress responses enhance its resilience in challenging conditions. The understanding of S. enterica versatility is crucial for public health, because non-traditional hosts and unconventional habitats multiply the potential sources of infection. Furthermore, the ability of Salmonella to persist in diverse environments necessitates a holistic approach in order to prevent infections, involving not only traditional clinical interventions but also strategies targeting the environmental reservoirs.

The study by Han et al. explores S. enterica adaptation to agricultural environments. These environments, including soil and crop plants, serve as ecological niches for Salmonella and act as vectors for its transmission to the consumer. This study specifically investigated the adaptation strategy of S. enterica serovar Typhimurium, analyzing glycolysis and the tricarboxylic acid pathway intermediates in diverse agricultural settings. The authors identified several crucial genes, such as aceE and aceB, associated with Salmonella Typhimurium persistence in root or leaf tissues. In vivo persistence assays in tomato leaves further confirmed the significance of these genes in allowing Salmonella Typhimurium to adapt to agricultural environments. Additionally, the researchers unveiled a compensatory mechanism involving fumarate accumulation in response to mutations in a specific gene, aceB. These findings provide valuable insights into the complex mechanisms employed by Salmonella Typhimurium to regulate its metabolism in response to the diverse carbon sources present in agricultural habitats. Understanding these adaptation strategies seems crucial for developing effective strategies to reduce Salmonella persistence in food production systems, contributing to improved food safety.

The versatility of Salmonella Typhimurium in the colonization of different ecological niches depends also on its ability to respond efficiently to the fluctuation in micronutrient availability. Among these, zinc (Zn) plays an essential role in bacterial physiology. Although it is well-established that animals employ Zn nutritional immunity strategies to fend off pathogens, it is unknown if Zn is involved in Salmonella-plant interactions. In the study by Visconti et al., authors investigated the involvement of Salmonella Typhimurium Zn/Cd export systems in plant colonization using Arabidopsis thaliana as the model host. The authors demonstrated that Salmonella persistence in plant tissues was influenced by the Zn content and that, above a certain concentration, Salmonella expression of metal efflux pumps ZntA and ZitB was required for its survival in plants. The study intriguingly observed that the bacterial advantage in Zn detoxification becomes more pronounced in plant colonization under elevated Zn availability. Furthermore, this study revealed a fascinating aspect: the bacterial disadvantage associated with impaired Zn detoxification can be mitigated if the plant fails to efficiently translocate Zn to the shoots. This highlighted the intricate balance in Salmonella-plant interactions, where both bacterial adaptation strategies and host ability to transport Zn influenced the outcome. Importantly, the study proposed a potential strategy to control pathogen colonization via biofortification: namely by modulating plant metal content. Manipulation of the Zn level in plants could be an effective means of inhibiting Salmonella colonization.

In the context of food safety, the study by Liao et al. presents a promising approach to address the challenge of seed contamination with foodborne pathogens, specifically mung bean seeds. The authors explored the biocontrol potential of Escherichia phage Sa157lw. The significance of this research lies in its innovative strategy to combat contamination with pathogenic Escherichia coli and various Salmonella serovars in sprout production, where susceptibility to antimicrobials and the escalating issue of antimicrobial resistance pose urgent concerns. The detailed characterization of a phage (Sa157lw), including whole-genome sequencing and biological assessments, provides a robust foundation for understanding its biocontrol potential. The application of Sa157lw on mung bean seeds demonstrated significant antimicrobial effects, as evidenced by the substantial reductions in both E. coli O157:H7 and Salmonella Typhimurium after storage. The research offers an innovative antimicrobial intervention, addressing the pressing need for effective strategies in the face of increasing antimicrobial resistance (AMR) and susceptibility challenges in sprout production.

The study by Guan et al. provides a comprehensive exploration of S. enterica in an unconventional habitat, namely waterfowl, shedding light on the dynamic nature of AMR and the potential public health risks associated with these avian hosts. The research, conducted in Sichuan, China, emphasized the scarcity of systematic studies on Salmonella prevalence in waterfowl species, despite their significance as major reservoirs and sources for Salmonella transmission. The recovery and characterization of Salmonella isolates from two distinct collection periods revealed a diversity of serovars harboring multidrug resistance patterns. Whole-genome sequencing unveiled a complex array of AMR genes, including efflux pump genes, specific resistance genes, and notable temporal variations in resistance patterns. The identification of resistance genes like tet(A)/tet(B) and catII in the first collection period and gyrA/gyrB mutations in the second period pointed to shifts in AMR genes over time. Moreover, the detection of incompatible plasmid replicon fragments highlighted the potential for horizontal transmission of AMR genes, contributing even further to the competitive advantage of Salmonella in highly diverse microbial habitats. This insight into the genetic diversity and adaptive mechanisms of Salmonella in waterfowl populations contributes crucial information for understanding the evolution of AMR and the associated risks to public health.

The genetic diversity of Salmonella isolates, collected in Shenzhen, China over an 11-year period of time, was analyzed in the study by Luo et al.. The research, using whole-genome sequencing and drug resistance phenotyping, explored population dynamics, inter-host relationships, drug resistance, and food-related transmission risks. The identification of two main sequence types, that are becoming increasingly prevalent in recent years, underscored the dynamic nature of Salmonella genetic diversity and its potential impact on public health.

In conclusion, the ability of Salmonella to thrive in unusual hosts and unconventional habitats highlights its remarkable adaptability. Exploring the molecular mechanisms and the genetic diversity behind this versatility is essential for developing effective preventive and control measures and predictive models. Therefore, our increasing understanding of Salmonella ecology renders the consideration of a broader spectrum of hosts and habitats essential, in order to comprehensively address the challenges posed by this pathogen to public health and microbial ecology.

Author contributions

SA: Writing – original draft, Writing – review & editing. SM: Writing – review & editing. AS: Writing – review & editing.

Funding

The author(s) declare that no financial support was received for the research, authorship, and/or publication of this article.

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.

The author(s) declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision.

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