AUTHOR=Braglia Chiara , Alberoni Daniele , Garrido Paula Melisa , Porrini Martin Pablo , Baffoni Loredana , Scott Dara , Eguaras Martin Javier , Di Gioia Diana , Mifsud David 

TITLE=Vairimorpha (Nosema) ceranae can promote Serratia development in honeybee gut: an underrated threat for bees?

JOURNAL=Frontiers in Cellular and Infection Microbiology

VOLUME=14

YEAR=2024

URL=https://www.frontiersin.org/journals/cellular-and-infection-microbiology/articles/10.3389/fcimb.2024.1323157

DOI=10.3389/fcimb.2024.1323157

ISSN=2235-2988

ABSTRACT=<p>The genus <italic>Serratia</italic> harbors opportunistic pathogenic species, among which <italic>Serratia marcescens</italic> is pathogenic for honeybees although little studied. Recently, virulent strains of <italic>S. marcescens</italic> colonizing the <italic>Varroa destructor</italic> mite’s mouth were found vectored into the honeybee body, leading to septicemia and death. <italic>Serratia</italic> also occurs as an opportunistic pathogen in the honeybee’s gut with a low absolute abundance. The <italic>Serratia</italic> population seems controlled by the host immune system, but its presence may represent a hidden threat, ready to arise when honeybees are weakened by biotic and abiotic stressors. To shed light on the <italic>Serratia</italic> pathogen, this research aims at studying <italic>Serratia</italic>’s development dynamics in the honeybee body and its interactions with the co-occurring fungal pathogen <italic>Vairimorpha ceranae</italic>. Firstly, the degree of pathogenicity and the ability to permeate the gut epithelial barrier of three <italic>Serratia</italic> strains, isolated from honeybees and belonging to different species (<italic>S. marcescens</italic>, <italic>Serratia liquefaciens</italic>, and <italic>Serratia nematodiphila</italic>), were assessed by artificial inoculation of newborn honeybees with different <italic>Serratia</italic> doses (10<sup>4</sup>, 10<sup>6</sup>, and 10<sup>8</sup> cells/mL). The absolute abundance of <italic>Serratia</italic> in the gut and in the hemocoel was assessed in qPCR with primers targeting the <italic>luxS</italic> gene. Moreover, the absolute abundance of <italic>Serratia</italic> was assessed in the gut of honeybees infected with <italic>V. ceranae</italic> at different development stages and supplied with beneficial microorganisms and fumagillin. Our results showed that all tested <italic>Serratia</italic> strains could pass through the gut epithelial barrier and proliferate in the hemocoel, with <italic>S. marcescens</italic> being the most pathogenic. Moreover, under cage conditions, <italic>Serratia</italic> better proliferates when a <italic>V. ceranae</italic> infection is co-occurring, with a positive and significant correlation. Finally, fumagillin and some of the tested beneficial microorganisms could control both <italic>Serratia</italic> and <italic>Vairimorpha</italic> development. Our findings suggest a correlation between the two pathogens under laboratory conditions, a co-occurring infection that should be taken into consideration by researches when testing antimicrobial compounds active against <italic>V. ceranae</italic>, and the related honeybees survival rate. Moreover, our findings suggest a positive control of <italic>Serratia</italic> by the environmental microorganism <italic>Apilactobacillus kunkeei</italic> in a in vivo model, confirming the potential of this specie as beneficial bacteria for honeybees.</p>