Deterministic Assembly of Complex Bacterial Communities in Guts of Germ-Free Cockroaches

Abstract

cThe gut microbiota of termites plays important roles in the symbiotic digestion of lignocellulose. However, the factors shaping the microbial community structure remain poorly understood. Because termites cannot be raised under axenic conditions, we established the closely related cockroach Shelfordella lateralis as a germ-free model to study microbial community assembly and host-microbe interactions. In this study, we determined the composition of the bacterial assemblages in cockroaches inoculated with the gut microbiota of termites and mice using pyrosequencing analysis of their 16S rRNA genes. Although the composition of the xenobiotic communities was influenced by the lineages present in the foreign inocula, their structure resembled that of conventional cockroaches. Bacterial taxa abundant in conventional cockroaches but rare in the foreign inocula, such as Dysgonomonas and Parabacteroides spp., were selectively enriched in the xenobiotic communities. Donor-specific taxa, such as endomicrobia or spirochete lineages restricted to the gut microbiota of termites, however, either were unable to colonize germ-free cockroaches or formed only small populations. The exposure of xenobiotic cockroaches to conventional adults restored their normal microbiota, which indicated that autochthonous lineages outcompete foreign ones. Our results provide experimental proof that the assembly of a complex gut microbiota in insects is deterministic.T ermites and cockroaches play important ecological roles in the turnover of lignocellulose in terrestrial ecosystems (1). These roles depend on the well-regulated nutritional relationships that they have evolved with their gut microbiota over millions of years (2). Compared to the gut microbiota associated with most other model insects, such as fruit flies (3) and bees (4), which are dominated by a few bacterial species, those of termites and cockroaches are considerably more diverse. Previous studies have shown that the composition of their gut microbiota reflects both the common evolutionary origin of and the dietary diversity within this group (5, 6), which makes them excellent models for investigating factors shaping complex gut communities in insects (7).Comparative analyses of the bacterial gut microbiota of termites and cockroaches have revealed that the influence of host taxonomy in community composition is overshadowed by that of host diet (6). A more recent study on higher termites also identified diet as the primary determinant shaping bacterial community structure (8) and hypothesized that differences in diet impact the availability of microhabitats to particular bacterial lineages. These results strongly suggest that the intestinal environment is a strong driver of microbial community structure in termite guts, but the validity of this hypothesis still remains to be experimentally tested.However, termites cannot be raised germ-free because of their obligate dependence on their gut microbiota. Also their elaborate social structure makes them intractable as gnotobiotic m...

Change in the intestinal bacterial community structure associated with environmental microorganisms during the growth of Eriocheir sinensis

“…Bacteroidetes has a corresponding abundance in the intestines of fish and shrimp (Baldo, Riera, Toomingklunderud, & Albà, 2015;Rungrassamee et al, 2014;Zhang, Sun, Chen, & Yu, 2014); however, its function has not been determined. The genus Dysgonomonas has a certain abundance in the gut of cockroaches and termites (Mikaelyan, Thompson, Hofer, & Brune, 2015). It is a common genus of termites intestines and plays an important role in assisting termites to digest lignocellulose, in immunity, and in reproduction (Brune, 2014;Fraune & Bosch, 2010;Scharf, 2015;Su, Yang, Huang, & Su, 2016;Warnecke, Luginbühl, Ivanova, & Ghassemian, 2007;Werren, Baldo, & Clark, 2008).…”

Community structure of the gut microbiota in sympatric species of wild Drosophila

“…; Mikaelyan et al . ), suggesting that the composition of the microbiota can be specific to the host species. Nevertheless, surveys have found substantial microbiota variation among individuals in many species and the processes by which the gut microbiota is assembled remain largely unknown (Falony et al .…”

“…Perturbations to the gut community can detrimentally affect the host, and some animals have evolved specific behaviours or gut morphologies to obtain and retain beneficial microbial associates (Engel & Moran 2013). Consistently associated sets of microbes have been described in several species of animals (Fraune & Bosch 2007;Martinson et al 2011;Berg et al 2016;Mikaelyan et al 2016), suggesting that the composition of the microbiota can be specific to the host species. Nevertheless, surveys have found substantial microbiota variation among individuals in many species and the processes by which the gut microbiota is assembled remain largely unknown (Falony et al 2016).…”

Co‐evolution of marine worms and their chemoautotrophic bacterial symbionts: unexpected host switches explained by ecological fitting?

“…; Mikaelyan et al . ), the exact mechanisms underlying the selection and maintenance of specific partners remain unclear. It is likely that the stability of such animal–microbe interactions is based on specific molecular mechanisms that allow recognition of cognate symbionts or exclusion of unwanted bacteria.…”

“…While ecological fitting can explain the diffuse co-evolution of host and symbionts observed in open symbioses, including the habitat-specific lineages that occur in the gut microbiota of mammals and insects (Seedorf et al 2014;Mikaelyan et al 2016), the exact mechanisms underlying the selection and maintenance of specific partners remain unclear. It is likely that the stability of such animal-microbe interactions is based on specific molecular mechanisms that allow recognition of cognate symbionts or exclusion of unwanted bacteria.…”