RESUMO
Biofilm formation is a common adaptation enabling bacteria to thrive in various environments and withstand external pressures. In the context of host-microbe interactions, biofilms play vital roles in establishing microbiomes associated with animals and plants and are used by opportunistic microbes to facilitate survival within hosts. Investigating biofilm dynamics, composition, and responses to environmental stressors is crucial for understanding microbial community assembly and biofilm regulation in health and disease. In this study, we explore in vivo colonization and in vitro biofilm formation abilities of core members of the honey bee (Apis mellifera) gut microbiota. Additionally, we assess the impact of glyphosate, a widely used herbicide with antimicrobial properties, and a glyphosate-based herbicide formulation on growth and biofilm formation in bee gut symbionts as well as in other biofilm-forming bacteria associated with diverse animals and plants. Our results demonstrate that several strains of core bee gut bacterial species can colonize the bee gut, which probably depends on their ability to form biofilms. Furthermore, glyphosate exposure elicits variable effects on bacterial growth and biofilm formation. In some instances, the effects correlate with the bacteria's ability to encode a susceptible or tolerant version of the enzyme inhibited by glyphosate in the shikimate pathway. However, in other instances, no such correlation is observed. Testing the herbicide formulation further complicates comparisons, as results often diverge from glyphosate exposure alone, suggesting that co-formulants influence bacterial growth and biofilm formation. These findings highlight the nuanced impacts of environmental stressors on microbial biofilms, with both ecological and host health-related implications. IMPORTANCE: Biofilms are essential for microbial communities to establish and thrive in diverse environments. In the honey bee gut, the core microbiota member Snodgrassella alvi forms biofilms, potentially aiding the establishment of other members and promoting interactions with the host. In this study, we show that specific strains of other core members, including Bifidobacterium, Bombilactobacillus, Gilliamella, and Lactobacillus, also form biofilms in vitro. We then examine the impact of glyphosate, a widely used herbicide that can disrupt the bee microbiota, on bacterial growth and biofilm formation. Our findings demonstrate the diverse effects of glyphosate on biofilm formation, ranging from inhibition to enhancement, reflecting observations in other beneficial or pathogenic bacteria associated with animals and plants. Thus, glyphosate exposure may influence bacterial growth and biofilm formation, potentially shaping microbial establishment on host surfaces and impacting health outcomes.
RESUMO
Honey bees are important agricultural pollinators that rely on a specific gut microbiota for the regulation of their immune system and defense against pathogens. Environmental stressors that affect the bee gut microbial community, such as antibiotics and glyphosate, can indirectly compromise bee health. Most of the experiments demonstrating these effects have been done under laboratory conditions with pure chemicals. Here, we investigated the oral and topical effects of various concentrations of glyphosate in a herbicide formulation on the honey bee gut microbiota and health under laboratory and field conditions. Under all of these conditions, the formulation, dissolved in sucrose syrup or water, affected the abundance of beneficial bacteria in the bee gut in a dose-dependent way. Mark-recapture experiments also demonstrated that bees exposed to the formulation were more likely to disappear from the colony, once reintroduced after exposure. Although no visible effects were observed for hives exposed to the formulation in field experiments, challenge trials with the pathogen Serratia marcescens, performed under laboratory conditions, revealed that bees from hives exposed to the formulation exhibited increased mortality compared with bees from control hives. In the field experiments, glyphosate was detected in honey collected from exposed hives, showing that worker bees transfer xenobiotics to the hive, thereby extending exposure and increasing the chances of exposure to recently emerged bees. These findings show that different routes of exposure to glyphosate-based herbicide can affect honey bees and their gut microbiota.IMPORTANCE The honey bee gut microbial community plays a vital role in immune response and defense against opportunistic pathogens. Environmental stressors, such as the herbicide glyphosate, may affect the gut microbiota, with negative consequences for bee health. Glyphosate is usually sprayed in the field mixed with adjuvants, which enhance herbicidal activity. These adjuvants may also enhance undesired effects in nontargeted organisms. This seems to be the case for glyphosate-based herbicide on honey bees. As we show in this study, oral exposure to either pure glyphosate or glyphosate in a commercial herbicide formulation perturbs the gut microbiota of honey bees, and topical exposure to the formulation also has a direct effect on honey bee health, increasing mortality in a dose-dependent way and leaving surviving bees with a perturbed microbiota. Understanding the effects of herbicide formulations on honey bees may help to protect these important agricultural pollinators.
