Classifying the bacterial gut microbiota of termites and cockroaches: A curated phylogenetic reference database (DictDb)

Mikaelyan, Aram; Köhler, Tim; Lampert, Niclas; Rohland, Jeffrey; Boga, Hamadi Iddi; Meuser, Katja; Brune, Andreas

doi:10.1016/j.syapm.2015.07.004

Cited by 83 publications

(142 citation statements)

References 60 publications

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“…For the analysis of taxonomic composition, a representative phylotype from each of the OTUs in a sample was classified with the RDP classifier (19) implemented in the mothur software suite (20) at a confidence cutoff of 80%, using DictDb v. 3.0 as reference database (13). Genus level lineages were ranked by determining their cumulative contribution to the principal component analysis of the gut communities as previously described (6,21).…”

Section: Methodsmentioning

confidence: 99%

“…In comparison, their closest relatives, the noneusocial cockroaches, do not depend on colony members for nourishment and can be raised in isolation under axenic conditions (9). Moreover, the physicochemical conditions in cockroach guts (5,10) are similar to those of many termites (11,12), which would offer a surrogate environment at least for those core lineages of gut microbiota that are shared with termites (5,6,13). These characteristics make cockroaches excellent models to experimentally test theories on the selective role of the insect gut environment in the assembly of the intestinal microbial community.…”

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confidence: 99%

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

Mikaelyan

Thompson

Höfer

et al. 2016

Appl Environ Microbiol

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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...

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Section: Methodsmentioning

confidence: 99%

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confidence: 99%

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

Mikaelyan

Thompson

Höfer

et al. 2016

Appl Environ Microbiol

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“…During recent years, the microbial community structure of many termites has been studied in detail, and the evolutionary patterns in the gut microbiota of termites and their closest phylogenetic relatives, the cockroaches, are slowly emerging (3). In particular, the application of high-throughput sequencing techniques provides sufficient resolution and sampling depth to distinguish the phylogenetic and environmental drivers of the community structure (4,5,6).The functional roles of individual community members and their interactions, however, are more difficult to elucidate, mostly due to their formidable resistance to cultivation. Metagenomic and metatranscriptomic approaches have provided the first insights into the functional potentials of the gut community (7,8,9), but owing to the lack of reference genomes for many deepbranching lineages of the gut microbiota, it remains difficult to assign functional genes to particular members of the respective communities.…”

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confidence: 99%

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Oxygen Affects Gut Bacterial Colonization and Metabolic Activities in a Gnotobiotic Cockroach Model

Tegtmeier

Thompson

Schauer

et al. 2016

Appl Environ Microbiol

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The gut microbiota of termites and cockroaches represents complex metabolic networks of many diverse microbial populations. The distinct microenvironmental conditions within the gut and possible interactions among the microorganisms make it essential to investigate how far the metabolic properties of pure cultures reflect their activities in their natural environment. We established the cockroach Shelfordella lateralis as a gnotobiotic model and inoculated germfree nymphs with two bacterial strains isolated from the guts of conventional cockroaches. Fluorescence microscopy revealed that both strains specifically colonized the germfree hindgut. In diassociated cockroaches, the facultatively anaerobic strain EbSL (a new species of Enterobacteriaceae) always outnumbered the obligately anaerobic strain FuSL (a close relative of Fusobacterium varium), irrespective of the sequence of inoculation, which showed that precolonization by facultatively anaerobic bacteria does not necessarily favor colonization by obligate anaerobes. Comparison of the fermentation products of the cultures formed in vitro with those accumulated in situ indicated that the gut environment strongly affected the metabolic activities of both strains. The pure cultures formed the typical products of mixed-acid or butyrate fermentation, whereas the guts of gnotobiotic cockroaches accumulated mostly lactate and acetate. Similar shifts toward more-oxidized products were observed when the pure cultures were exposed to oxygen, which corroborated the strong effects of oxygen on the metabolic fluxes previously observed in termite guts. Oxygen microsensor profiles of the guts of germfree, gnotobiotic, and conventional cockroaches indicated that both gut tissue and microbiota contribute to oxygen consumption and suggest that the oxygen status influences the colonization success. M any insects, particularly those feeding on a fiber-rich diet, possess a dense and complex microbiota. The most prominent examples are termites, whose ability to thrive on an entirely lignocellulosic diet depends on the digestive and nutritional contributions of microbial symbionts housed in their intestinal tracts (1, 2). During recent years, the microbial community structure of many termites has been studied in detail, and the evolutionary patterns in the gut microbiota of termites and their closest phylogenetic relatives, the cockroaches, are slowly emerging (3). In particular, the application of high-throughput sequencing techniques provides sufficient resolution and sampling depth to distinguish the phylogenetic and environmental drivers of the community structure (4,5,6).The functional roles of individual community members and their interactions, however, are more difficult to elucidate, mostly due to their formidable resistance to cultivation. Metagenomic and metatranscriptomic approaches have provided the first insights into the functional potentials of the gut community (7,8,9), but owing to the lack of reference genomes for many deepbranching lineages of the gut microbiot...

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“…In higher termites, Spirochaetes, 'Candidatus phylum TG3' and Fibrobacteres are the dominant groups. Distinct termite species harbor different bacterial species with community structures specific to the host species, but most of those bacteria belong to phylogenetic clades that are unique to termites and are shared among diverse termite species (Hongoh 2010;Mikaelyan et al 2015). While Firmicutes and Bacteroidetes are generally more abundant in cockroaches than in termites, Spirochaetes are absent or have yet to be described in omnivorous cockroaches.…”

Section: Gregarious and Social Dictyopteramentioning

confidence: 99%

The holobiont concept: the case of xylophagous termites and cockroaches

Berlanga

Guerrero

2016

Symbiosis

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The rapid growth in microbiome research, particularly during the last 15 years, has revealed the crucial contributions of microbial communities to numerous physiological functions in animals, including digestion, immunity and reproduction.The permanent coexistence of these various bionts forms the holobiont (namely, the host and its microbiota). This review describes the relationships between xylophagous insects and their microbiota in an attempt to understand the characteristics that have determined bacterial fidelity over generations and throughout evolutionary history.Symbiotic interactions have probably played a central role in the evolutionary success of these insects, allowing their adaptation to unexploited ecological niches that are nutritionally deficient and/or unbalanced. Moreover, insect symbionts have provided the enzymatic capabilities that enable the synthesis of nutrients (carbon and nitrogen sources for the host) from recalcitrant plant polymers (cellulose, hemicellulose, pectin or lignin).

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Classifying the bacterial gut microbiota of termites and cockroaches: A curated phylogenetic reference database (DictDb)

Cited by 83 publications

References 60 publications

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

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

Oxygen Affects Gut Bacterial Colonization and Metabolic Activities in a Gnotobiotic Cockroach Model

The holobiont concept: the case of xylophagous termites and cockroaches

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