Comparative Metagenomic and Metatranscriptomic Analysis of Hindgut Paunch Microbiota in Wood- and Dung-Feeding Higher Termites

He, Shaomei; Ivanova, Natalia; Kirton, Edward; Allgaier, Martin; Bergin, Claudia; Scheffrahn, Rudolf H.; Kyrpides, Nikos C.; Warnecke, Falk; Tringe, Susannah G.; Hugenholtz, Philip

doi:10.1371/journal.pone.0061126

Cited by 147 publications

(228 citation statements)

References 66 publications

(112 reference statements)

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“…1) (19). All other FDH lineages observed in other termites and the related wood roach, including those associated with spirochetes here or in other studies (11,13,19), are absent, and metagenomic analyses of higher termite gut communities (12,34) have identified no alternative FDH candidates. Thus, to date, ZnD2sec-like FDHs remain the sole candidate genes in higher termites for an important step in CO 2 -reductive acetogenesis known to occur at high rates in all woodfeeding, higher termites examined (12,35).…”

Section: Discussionmentioning

confidence: 43%

Localizing transcripts to single cells suggests an important role of uncultured deltaproteobacteria in the termite gut hydrogen economy

Rosenthal

Zhang

Lucey

et al. 2013

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

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Identifying microbes responsible for particular environmental functions is challenging, given that most environments contain an uncultivated microbial diversity. Here we combined approaches to identify bacteria expressing genes relevant to catabolite flow and to locate these genes within their environment, in this case the gut of a "lower," wood-feeding termite. First, environmental transcriptomics revealed that 2 of the 23 formate dehydrogenase (FDH) genes known in the system accounted for slightly more than one-half of environmental transcripts. FDH is an essential enzyme of H 2 metabolism that is ultimately important for the assimilation of lignocellulose-derived energy by the insect. Second, single-cell PCR analysis revealed that two different bacterial types expressed these two transcripts. The most commonly transcribed FDH in situ is encoded by a previously unappreciated deltaproteobacterium, whereas the other FDH is spirochetal. Third, PCR analysis of fractionated gut contents demonstrated that these bacteria reside in different spatial niches; the spirochete is free-swimming, whereas the deltaproteobacterium associates with particulates. Fourth, the deltaproteobacteria expressing FDH were localized to protozoa via hybridization chain reaction-FISH, an approach for multiplexed, spatial mapping of mRNA and rRNA targets. These results underscore the importance of making direct vs. inference-based genespecies associations, and have implications in higher termites, the most successful termite lineage, in which protozoa have been lost from the gut community. Contrary to expectations, in higher termites, FDH genes related to those from the protozoan symbiont dominate, whereas most others were absent, suggesting that a successful gene variant can persist and flourish after a gut perturbation alters a major environmental niche.acetogenesis | RNA-Seq | microfluidic digital PCR

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Section: Discussionmentioning

confidence: 43%

Localizing transcripts to single cells suggests an important role of uncultured deltaproteobacteria in the termite gut hydrogen economy

Rosenthal

Zhang

Lucey

et al. 2013

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

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“…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. Improved binning strategies promise a solution for this problem in the near future (10), but the elucidation of emergent community properties, such as specific interactions or metabolic networks, requires an entirely different approach.…”

mentioning

confidence: 99%

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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“…With the revolution of "omics" technologies, it is interesting to apply advanced studies on termites such as metagenomics, transcriptomics or proteomics [7][8][9]. These technologies offer the possibility to improve the screening for new enzymes and to study the system as a whole.…”

Section: Introductionmentioning

confidence: 99%

GC×GC-TOFMS for the Analysis of Metabolites Produced by Termites (Reticulitermes flavipes) Bred on Different Carbon Sources

et al. 2016

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Abstract:More and more studies are dedicated to termites and their symbionts, to better understand how they efficiently produce energy from lignocellulose. In that context, a powerful analytical method was developed to perform the detection, separation and identification of compounds in the 1 µL fluid volume of the gut of the termite Reticulitermes flavipes. Comprehensive two-dimensional gas chromatography (GCˆGC) coupled to time-of-flight mass spectrometry (TOFMS) was tested with three different column combinations: (1) low-polar/mid-polar; (2) polar/low-polar and (3) mid-polar/low-polar. The column set (3) offered the best separation and was chosen for further analysis and comparison study. Metabolites were detected in the samples, including amino acids, sugars, amines and organic acids. Samples collected from termites fed for 30 days on Avicel cellulose or xylan powder diets were analyzed and compared with the wood diet. Principal component analysis (PCA) of metabolite profiles demonstrated a separation of different clusters corresponding to the three different diets, with a similar trend for diets containing cellulose. The Analysis of variance (ANOVA) (one way-ANOVA and Tukey's test) was used to compare compound levels between these three different diets. Significant differences were observed, including higher levels of aromatic derivatives in the wood diet and higher levels of sugar alcohols in the xylan diet. A higher accumulation of uric acid was observed with the artificial diets (cellulose and xylan), likely to be related to the nitrogen deficiency. The present study highlighted the capability of adaptation of the termite system to non-optimal carbon sources and the subsequent modification of the metabolite profile. These results demonstrate the potential interest to investigate metabolite profiling with state-of-the-art separation science tools, in order to extract information that could be integrated with other omics data to provide more insight into the termite-symbiont digestion system.

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Comparative Metagenomic and Metatranscriptomic Analysis of Hindgut Paunch Microbiota in Wood- and Dung-Feeding Higher Termites

Cited by 147 publications

References 66 publications

Localizing transcripts to single cells suggests an important role of uncultured deltaproteobacteria in the termite gut hydrogen economy

Localizing transcripts to single cells suggests an important role of uncultured deltaproteobacteria in the termite gut hydrogen economy

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

GC×GC-TOFMS for the Analysis of Metabolites Produced by Termites (Reticulitermes flavipes) Bred on Different Carbon Sources

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