Niche heterogeneity determines bacterial community structure in the termite gut (<i>Reticulitermes santonensis</i>)

Yang, Hong; Schmitt-Wagner, Dirk; Stingl, Ulrich; Brune, Andreas

doi:10.1111/j.1462-2920.2005.00760.x

Cited by 132 publications

(110 citation statements)

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“…Bacteroidetes were found in low concentrations (1 %) in R. lucifugus, in contrast to the abundance found in Reticulitermes santonensis (Feytaud) (Yang et al 2005) and R. flavipes (Boucias et al 2013). Members of the phylum Bacteroidetes have been reported to reside in the gut as ecto-or endosymbionts of flagellated protozoa (Noda et al 2005;Nakajima et al 2006), and cellularlevel symbioses between Bacteroidales and gut protists are as common as those between spirochetes and gut protists.…”

Section: Resultsmentioning

confidence: 69%

“…Delta-proteobacteria have been recognised as playing a major role in the H 2 +CO 2 economy of termite hindgut communities; nitrogen-fixing Desulfovibrio strains have been isolated from the gut of termites (Ohkuma et al 1996;Sato et al 2009). Spirochaetes are a major constituent of wood-feeding termite gut microbiota (Lilburn et al 1999;Leadbetter et al 1999), both in lower (Yang et al 2005) and higher termites (Paster et al 1996;Warnecke et al 2007). In contrast, the population of Spirochaetes in the gut of fungus-growing and soil-feeding termites is lower SchmittWagner et al 2003) or absent (Shinzato et al 2007).…”

Section: Resultsmentioning

confidence: 99%

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The gut microbiota of the wood-feeding termite Reticulitermes lucifugus (Isoptera; Rhinotermitidae)

et al. 2015

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Termite gut is host to a complex microbial community consisting of prokaryotes, and in some cases flagellates, responsible for the degradation of lignocellulosic material. Here we report data concerning the analysis of the gut microbiota of Reticulitermes lucifugus (Rossi), a lower termite species that lives in underground environments and is widespread in Italy, where it causes damage to wood structures of historical and artistic monuments. A 16S rRNA gene clone library revealed that the R. lucifugus gut is colonized by members of five phyla in the domain Bacteria: Firmicutes (49 % of clones), Proteobacteria (24 %), Spirochaetes (14 %), the candidatus TG1 phylum (12 %), and Bacteroidetes (1 %). A collection of cellulolytic aerobic bacteria was isolated from the gut of R. lucifugus by enrichment cultures on different cellulose and lignocellulose substrates. Results showed that the largest amount of culturable cellulolytic bacteria of R. lucifugus belongs to Firmicutes in the genera Bacillus and Paenibacillus (67 %). These isolates are also able to grow on xylan and show the largest clear zone diameter in the Congo red test. Reticulitermes lucifugus hosts a diverse community of bacteria and could be considered an acceptable source of hydrolytic enzymes for biotechnological applications.

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Section: Resultsmentioning

confidence: 69%

Section: Resultsmentioning

confidence: 99%

The gut microbiota of the wood-feeding termite Reticulitermes lucifugus (Isoptera; Rhinotermitidae)

et al. 2015

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“…Reticulitermes spp (Hongoh et al, 2003;Yang et al, 2005). In addition, potential rates of sulfate reduction in gut homogenates of Mastotermes darwiniensis suggest a hydrogen turnover of o0.1% of the respiratory electron flow even when termites were fed a sulfate-enriched diet (calculated from data in Sugimoto et al, 1998 andDrö ge et al, 2005).…”

Section: Hydrogen Metabolism In Termite Guts M Pester and A Brunementioning

confidence: 99%

Hydrogen is the central free intermediate during lignocellulose degradation by termite gut symbionts

2007

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The key role of free hydrogen in the digestion of lignocellulose by wood-feeding lower termites and their symbiotic gut microbiota has been conceptually outlined in the past decades but remains to be quantitatively analyzed in situ. Using Reticulitermes santonensis, Zootermopsis nevadensis and Cryptotermes secundus, we determined metabolite fluxes involved in hydrogen turnover and the resulting distribution of H 2 in the microliter-sized gut. High-resolution hydrogen microsensor profiles revealed pronounced differences in hydrogen accumulation among the species (from o1 kPa to the saturation level). However, flux measurements indicated that the hydrogen pool was rapidly turned over in all termites, irrespective of the degree of accumulation. Microinjection of radiotracers into intact guts confirmed that reductive acetogenesis from CO 2 dominated hydrogen consumption, whereas methanogenesis played only a minor role. Only negligible amounts of H 2 were lost by emission, documenting an overall equilibrium between hydrogen production and consumption within the gut. Mathematical modeling revealed that production dominates in the gut lumen and consumption in the gut periphery for R. santonensis and Z. nevadensis, explaining the large accumulation of H 2 in these termites, whereas the moderate hydrogen accumulation in C. secundus indicated a more balanced radial distribution of the two processes. Daily hydrogen turnover rates were 9-33 m 3 H 2 per m 3 hindgut volume, corresponding to 22-26% of the respiratory activity of the termites. This makes H 2 the central free intermediate during lignocellulose degradation and the termite gut-with its high rates of reductive acetogenesis-the smallest and most efficient natural bioreactor currently known. The ISME Journal (2007) 1, 551-565; doi:10.1038/ismej.2007 IntroductionTermites inhabit about two-thirds of Earth's terrestrial surface and play important roles in the global carbon cycle (Lee and Wood, 1971;Wood and Sands, 1978;Collins and Wood, 1984;Sanderson, 1996;Bignell and Eggleton, 2000). Recently, wood-feeding termites received additional attention because lignocellulose degradation by their symbiotic gut microbiota presumably produces large amounts of hydrogen, an emerging 'clean' energy carrier (Dunn, 2002).Lignocellulose is the most abundant renewable resource of the biosphere. It consists mainly of cellulose and hemicelluloses, both of which are degraded with high efficiency during gut passage by the termite (65-99%, reviewed in Breznak and Brune, 1994). Although termites secrete their own cellulases and hemicellulases into foregut and midgut (Inoue et al., 1997;Watanabe and Tokuda, 2001;Tokuda et al., 2004Tokuda et al., , 2005, it is generally accepted that most of the polysaccharide degradation in lower termites occurs in the enlarged hindgut (Inoue et al., 1997;Tokuda et al., 2005), a bioreactorlike compartment with increased retention time and tightly packed with microorganisms (Breznak and Brune, 1994;Brune, 1998).In lower termites, the hindgut microbiota compr...

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“…To this aim, several recent studies have supported the "neutral hypothesis" (6)(7)(8), a largely stochastic model for community assembly, which assumes that species are ecologically equivalent and that community structure is determined by random processes (9,10). However, there is also evidence that niche or deterministic processes play a role in community structure (11,12); thus, both niche and neutral processes are likely to affect the assembly of complex microbial communities.…”

mentioning

confidence: 99%

Bacterial community assembly based on functional genes rather than species

Burke¹,

Steinberg

Rusch

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

728

606

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The principles underlying the assembly and structure of complex microbial communities are an issue of long-standing concern to the field of microbial ecology. We previously analyzed the community membership of bacterial communities associated with the green macroalga Ulva australis, and proposed a competitive lottery model for colonization of the algal surface in an attempt to explain the surprising lack of similarity in species composition across different algal samples. Here we extend the previous study by investigating the link between community structure and function in these communities, using metagenomic sequence analysis. Despite the high phylogenetic variability in microbial species composition on different U. australis (only 15% similarity between samples), similarity in functional composition was high (70%), and a core of functional genes present across all algal-associated communities was identified that were consistent with the ecology of surface-and hostassociated bacteria. These functions were distributed widely across a variety of taxa or phylogenetic groups. This observation of similarity in habitat (niche) use with respect to functional genes, but not species, together with the relative ease with which bacteria share genetic material, suggests that the key level at which to address the assembly and structure of bacterial communities may not be "species" (by means of rRNA taxonomy), but rather the more functional level of genes.lateral gene transfer | biofilm | ecological model M etagenomic analysis of environmental microbial communities has revealed an enormous and previously unknown microbial diversity, and expanded our knowledge of their function in a variety of environments (1-5). Much still remains unknown, however, such as the principles underlying the assembly and structure of complex microbial communities, an issue of long-standing concern to the field of microbial ecology. To this aim, several recent studies have supported the "neutral hypothesis" (6-8), a largely stochastic model for community assembly, which assumes that species are ecologically equivalent and that community structure is determined by random processes (9, 10). However, there is also evidence that niche or deterministic processes play a role in community structure (11, 12); thus, both niche and neutral processes are likely to affect the assembly of complex microbial communities.Support for these models is based on species abundance distributions, and critical functional aspects, such as the assumption of ecological equivalence, have for the most part not been tested. In this study, we examine the encoded functions of an algalassociated bacterial community and link patterns of function to patterns of community assembly. Following the results of an earlier study (13), we investigate these communities in the context of the lottery hypothesis, a model for community "assembly" derived from studies of eukaryotic communities, such as coral reef fish (14). This hypothesis incorporates both neutral and functional aspects and arg...

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Niche heterogeneity determines bacterial community structure in the termite gut (Reticulitermes santonensis)

Cited by 132 publications

References 63 publications

The gut microbiota of the wood-feeding termite Reticulitermes lucifugus (Isoptera; Rhinotermitidae)

The gut microbiota of the wood-feeding termite Reticulitermes lucifugus (Isoptera; Rhinotermitidae)

Hydrogen is the central free intermediate during lignocellulose degradation by termite gut symbionts

Bacterial community assembly based on functional genes rather than species

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