Niche partitioning facilitates coexistence of closely related gut bacteria

Abstract

Ecological processes underlying bacterial coexistence in the gut are not well understood. Here, we disentangled the effect of the host and the diet on the coexistence of four closely related Lactobacillus species colonizing the honey bee gut. We serially passaged the four species through gnotobiotic bees and in liquid cultures in the presence of either pollen (bee diet) or simple sugars. Although the four species engaged in negative interactions, they were able to stably coexist, both in vivo and in vitro. However, coexistence was only possible in the presence of pollen, but not in simple sugars independent of the environment. Using metatranscriptomics and metabolomics, we found that the four species utilize different pollen-derived carbohydrate substrates indicating resource partitioning as the basis of coexistence. Our results show that despite longstanding symbiotic associations, gut bacterial interactions can be recapitulated in vitro providing insights about bacterial coexistence when combined with in vivo experiments.

In their sister’s footsteps: Taxonomic divergence obscures substantial functional overlap among the metabolically diverse symbiotic gut communities of adult and larval turtle ants

“…The citrate transporter-encoding gene ( citT ) was annotated as a citrate:succinate antiporter [129], which coincides with, on the same scaffold, a cluster of genes coding for all the subunits of succinate dehydrogenase, involved in the reversible production of succinate. Our results show that only turtle ant larval symbionts can ferment pyruvate to formate, but both life stages host gut symbionts that have the genetic potential to ferment pyruvate into lactate and acetate, and share the putative citrate-fermenting Rhizobiales, which may be of use in pollen digestion [130].…”

“…Citrate could also be a pollen derivative, or produced as a downstream metabolite from enzymatic pathways catabolizing pollen-derived carbohydrates. Interestingly, genes involved in citrate fermentation in two honeybee-isolated Lactobacillus strains are activated in the presence of pollen [130]. The JR021-5/Bin10 symbiont also has the genetic ability to synthesize riboflavin and cobalamin-like corrinoids.…”

Global composition of the bacteriophage community in honeybees

“…It was recently shown that closely related strains of Lactobacillus nr. melliventris coexist in the honeybee gut through niche partitioning of pollen metabolism (65). Whether or not phages specialize on these functionally divergent bacteria and if phage host range evolution affects these bacterial communities remains an interesting question.…”

Social Interaction is Unnecessary for Hindgut Microbiome Transmission in Honey Bees: the Effect of Diet and Social Exposure on Tissue-Specific Microbiome Assembly

“…Lactobacillus firm5 is found with high prevalence and abundance throughout the hive environment and is readily acquired with natural eclosion [9,17,20,84]. It also dominates the hindgut microbiota and is a functionally variable phylotype thought to include at least four gut prevalent species (Brochet et al 2021). Based on detailed genome analysis from two locations, four functionally different species of the Lactobacillus firm5 phylotype are abundant in every hindgut, and hypothesized to coexist via resource partitioning [85].…”

“…It also dominates the hindgut microbiota and is a functionally variable phylotype thought to include at least four gut prevalent species (Brochet et al 2021). Based on detailed genome analysis from two locations, four functionally different species of the Lactobacillus firm5 phylotype are abundant in every hindgut, and hypothesized to coexist via resource partitioning [85]. Although less precise, our unique sequence analysis based on distinct gut regions supports the coexistence of 2-4 major strains of firm5 in the hindgut, but also suggests that Lactobacillus firm5 may associate by niche.…”