An interaction between host and microbe genotypes determines colonization success of a key bumble bee gut microbiota member

Abstract

There has been a proliferation of studies demonstrating an organism's health is influenced by its microbiota. However, factors influencing beneficial microbe colonization and the evolution of these relationships remain understudied relative to host–pathogen interactions. Vertically transmitted beneficial microbes are predicted to show high levels of specificity in colonization, including genotype matching, which may transpire through coevolution. We investigate how host and bacterial genotypes influence colonization of a core coevolved microbiota member in bumble bees. The hindgut colonizing Snodgrassella alvi confers direct benefits, but, as an early colonizer, also facilitates the further development of a healthy microbiota. Due to predominantly vertical transmission promoting tight evolution between colonization factors of bacteria and host lineages, we predict that genotype‐by‐genotype interactions will determine successful colonization. Germ‐free adult bees from seven bumble bee colonies (host genotypic units) were inoculated with one of six genetically distinct strains of S. alvi. Subsequent colonization within host and microbe genotypes combinations ranged from 0 to 100%, and an interaction between host and microbe genotypes determined colonization success. This novel finding of a genotype‐by‐genotype interaction determining colonization in an animal host‐beneficial microbe system has implications for the ecological and evolutionary dynamics of host and microbe, including associated host‐fitness benefits.

The red flour beetle Tribolium castaneum: A model for host-microbiome interactions

“…If bacteria are continually flushed out of the gut, they can only be replenished via food; and variation in microbial loads across individuals may simply reflect variation in the timing of when they last consumed flour. Alternatively, variation across individuals may also reflect host genotype-or condition-dependent bacterial colonization [35,36]. We hope that future experiments can distinguish between these hypotheses and determine the cause of large individual variation in the microbiome.…”

The effects of taxonomy, diet, and ecology on the microbiota of riverine macroinvertebrates

“…The processes by which core microbiota develop in invertebrates are not known; however, previous studies of terrestrial invertebrates point to several factors that may contribute to their formation and maintenance. Vertical transmission of bacteria from parent to offspring is supported by studies investigating the effects of taxonomy on the microbiota in cockroaches (Kakumanu et al., 2018; Sabree et al., 2012; Sabree & Moran, 2014), bumble bees (Koch et al., 2013; Kwong & Moran, 2015; Sauers & Sadd, 2019), honey bees (Koch et al., 2013; Kwong & Moran, 2015), and termites (Sabree et al., 2012; Sabree & Moran, 2014). Each of these invertebrates are found to feature specific bacterial species within their core microbiota that are observed consistently across all individuals regardless of diet, suggesting that particular bacteria have been passed down vertically from parent to offspring.…”

“…P values depicting significant differences in beta diversity are bolded. Effect size (R 2 ) values display how much of the overall variation in dissimilarities can be explained by the factor being tested (Kakumanu et al, 2018;Sabree et al, 2012;Sabree & Moran, 2014), bumble bees (Koch et al, 2013;Kwong & Moran, 2015;Sauers & Sadd, 2019), honey bees (Koch et al, 2013;Kwong & Moran, 2015), and termites (Sabree et al, 2012;Sabree & Moran, 2014). Each of these invertebrates are found to feature specific bacterial species within their core microbiota that are observed consistently across all individuals regardless of diet, suggesting that particular bacteria have been passed down vertically from parent to offspring.…”

“…Overall, these studies have revealed that microbiota are shaped by host taxonomy (Colman et al., 2012; Jones et al., 2013; Mikaelyan et al., 2015; Muturi et al., 2017; Singhal et al., 2017; Yun et al., 2014), environmental changes (Yun et al., 2014), and contaminants (Pennington et al., 2017), and the health of the host is often affected when these bacteria become severely disrupted, as is seen in dysbiosis (Clark & Walker, 2018; Hamdi et al., 2011; Raymann & Moran, 2018). Specifically, studies targeting host taxonomy have found that distinct bacterial taxa are exclusively limited to certain terrestrial invertebrate genera belonging to orders such as Blattodea (cockroaches and termites) (Colman et al., 2012; Kakumanu et al., 2018; Sabree et al., 2012; Sabree & Moran, 2014) and Hymenoptera (ants, bees, and wasps) (Colman et al., 2012; Koch et al, 2013; Kwong & Moran, 2015; Sauers & Sadd, 2019); measures of alpha diversity such as bacterial richness and evenness were also shown to differ significantly among eight invertebrate orders, with alpha diversity measures showing greater similarity among closely related invertebrates (Jones et al., 2013). A previous study comparing microbiota across varying habitats showed significant differences in the relative abundance of anaerobic bacteria, but not in aerobic or facultative anaerobic bacteria (Yun et al., 2014).…”

“…Specifically, studies targeting host taxonomy have found that distinct bacterial taxa are exclusively limited to certain terrestrial invertebrate genera belonging to orders such as Blattodea (cockroaches and termites) (Colman et al, 2012;Kakumanu et al, 2018;Sabree et al, 2012;Sabree & Moran, 2014) and Hymenoptera (ants, bees, and wasps) (Colman et al, 2012;Koch et al, 2013;Kwong & Moran, 2015;Sauers & Sadd, 2019); measures of alpha diversity such as bacterial richness and evenness were also shown to differ significantly among eight invertebrate orders, with alpha diversity measures showing greater similarity among closely related invertebrates (Jones et al, 2013). A previous study comparing microbiota across varying habitats showed significant differences in the relative abundance of anaerobic bacteria, but not in aerobic or facultative anaerobic bacteria (Yun et al, 2014).…”