SUMMARY To study how microbes establish themselves in a mammalian gut environment, we colonized germ-free mice with microbial communities from human, zebrafish and termite guts, human skin and tongue, soil, and estuarine microbial mats. Bacteria from these foreign environments colonized and persisted in the mouse gut; their capacity to metabolize dietary and host carbohydrates, and bile acids, correlated with colonization success. Co-housing mice harboring these xenomicrobiota with one another, with mice harboring native gut microbiota, and germ-free ‘bystanders’ revealed the success of particular bacterial taxa in colonizing an empty gut habitat and guts with established communities. Unanticipated patterns of ecological succession were observed; for example, a soil-derived bacterium dominated even in the presence of bacteria from other gut communities (zebrafish and termite), and human-derived bacteria colonized germ-free mice before mouse-derived organisms. This approach generalizes to address a variety of mechanistic questions about succession, including succession in the context of microbiota-directed therapeutics.

Termites effectively feed on many types of lignocellulose assisted by their gut microbial symbionts. To better understand the microbial decomposition of biomass with varied chemical profiles, it is important to determine whether termites harbor different microbial symbionts with specialized functionalities geared toward different feeding regimens. In this study, we compared the microbiota in the hindgut paunch of Amitermes wheeleri collected from cow dung and Nasutitermes corniger feeding on sound wood by 16S rRNA pyrotag, comparative metagenomic and metatranscriptomic analyses. We found that Firmicutes and Spirochaetes were the most abundant phyla in A. wheeleri, in contrast to N. corniger where Spirochaetes and Fibrobacteres dominated. Despite this community divergence, a convergence was observed for functions essential to termite biology including hydrolytic enzymes, homoacetogenesis and cell motility and chemotaxis. Overrepresented functions in A. wheeleri relative to N. corniger microbiota included hemicellulose breakdown and fixed-nitrogen utilization. By contrast, glycoside hydrolases attacking celluloses and nitrogen fixation genes were overrepresented in N. corniger microbiota. These observations are consistent with dietary differences in carbohydrate composition and nutrient contents, but may also reflect the phylogenetic difference between the hosts.

ABSTRACTHigher termites are characterized by a purely prokaryotic gut microbiota and an increased compartmentation of their intestinal tract. In soil-feeding species, each gut compartment has different physicochemical conditions and is colonized by a specific microbial community. Although considerable information has accumulated also for wood-feeding species of the genusNasutitermes, including cellulase activities and metagenomic data, a comprehensive study linking physicochemical gut conditions with the structure of the microbial communities in the different gut compartments is lacking. In this study, we measured high-resolution profiles of H2, O2, pH, and redox potential in the gut ofNasutitermes cornigertermites, determined the fermentation products accumulating in the individual gut compartments, and analyzed the bacterial communities in detail by pyrotag sequencing of the V3-V4 region of the 16S rRNA genes. The dilated hindgut paunch (P3 compartment) was the only anoxic gut region, showed the highest density of bacteria, and accumulated H2to high partial pressures (up to 12 kPa). Molecular hydrogen is apparently produced by a dense community ofSpirochaetesandFibrobacteres, which also dominate the gut of otherNasutitermesspecies. All other compartments, such as the alkaline P1 compartment (average pH, 10.0), showed high redox potentials and comprised small but distinct populations characteristic for each gut region. In the crop and the posterior hindgut compartments, the community was even more diverse than in the paunch. Similarities in the communities of the posterior hindgut and crop suggested that proctodeal trophallaxis or coprophagy also occurs in higher termites. The large sampling depths of pyrotag sequencing in combination with the determination of important physicochemical parameters allow cautious conclusions concerning the functions of particular bacterial lineages in the respective gut sections to be drawn.

eThe hindguts of lower termites and Cryptocercus cockroaches are home to a distinct community of archaea, bacteria, and protists (primarily parabasalids and some oxymonads). Within a host species, the composition of these hindgut communities appears relatively stable, but the evolutionary and ecological factors structuring community composition and stability are poorly understood, as are differential impacts of these factors on protists, bacteria, and archaea. We analyzed the microbial composition of parabasalids and bacteria in the hindguts of Cryptocercus punctulatus and 23 species spanning 4 families of lower termites by pyrosequencing variable regions of the small-subunit rRNA gene. Especially for the parabasalids, these data revealed undiscovered taxa and provided a phylogenetic basis for a more accurate understanding of diversity, diversification, and community composition. The composition of the parabasalid communities was found to be strongly structured by the phylogeny of their hosts, indicating the importance of historical effects, although exceptions were also identified. Particularly, spirotrichonymphids and trichonymphids likely were transferred between host lineages. In contrast, host phylogeny was not sufficient to explain the majority of bacterial community composition, but the compositions of the Bacteroidetes, Elusimicrobia, Tenericutes, Spirochaetes, and Synergistes were structured by host phylogeny perhaps due to their symbiotic associations with protists. All together, historical effects probably resulting from vertical inheritance have had a prominent role in structuring the hindgut communities, especially of the parabasalids, but dispersal and environmental acquisition have played a larger role in community composition than previously expected.C ryptocercus cockroaches and their sister lineage, the lower termites (1), are both dependent on diverse communities of microorganisms in their hindguts to gain nutrition from lignocellulose (reviewed in references 2 and 3). These are fascinating and complex communities dominated by parabasalid (Parabasalia) and oxymonad (Preaxostyla) protists (4) as well as numerous bacterial lineages, including Actinobacteria, Bacteroidetes, Elusimicrobia, Firmicutes, Proteobacteria, Spirochaetes,. Moreover, a large proportion of the bacteria form obligate symbiotic interactions with the protists (see, for example, references 8-14), so the community contains multiple levels of symbiosis. Because of the diversity of symbionts, the hindguts of Cryptocercus cockroaches and lower termites can be used as model systems to study the ecology and interactions between protists and bacteria. Here, we investigate the ecological and evolutionary differences between protists and bacteria in structuring community composition. These differences are critical to understanding the diversification and adaptation of microbes, the stability and resilience of community structure, and the maintenance of ecosystem functions, particularly in regard to understanding lignocellulose digestion...

BackgroundTermites are important contributors to carbon and nitrogen cycling in tropical ecosystems. Higher termites digest lignocellulose in various stages of humification with the help of an entirely prokaryotic microbiota housed in their compartmented intestinal tract. Previous studies revealed fundamental differences in community structure between compartments, but the functional roles of individual lineages in symbiotic digestion are mostly unknown.ResultsHere, we conducted a highly resolved analysis of the gut microbiota in six species of higher termites that feed on plant material at different levels of humification. Combining amplicon sequencing and metagenomics, we assessed similarities in community structure and functional potential between the major hindgut compartments (P1, P3, and P4). Cluster analysis of the relative abundances of orthologous gene clusters (COGs) revealed high similarities among wood- and litter-feeding termites and strong differences to humivorous species. However, abundance estimates of bacterial phyla based on 16S rRNA genes greatly differed from those based on protein-coding genes.ConclusionCommunity structure and functional potential of the microbiota in individual gut compartments are clearly driven by the digestive strategy of the host. The metagenomics libraries obtained in this study provide the basis for future studies that elucidate the fundamental differences in the symbiont-mediated breakdown of lignocellulose and humus by termites of different feeding groups. The high proportion of uncultured bacterial lineages in all samples calls for a reference-independent approach for the correct taxonomic assignment of protein-coding genes.Electronic supplementary materialThe online version of this article (doi:10.1186/s40168-015-0118-1) contains supplementary material, which is available to authorized users.

Cryptotermes brevis is a common pest of structural lumber and sheltered wood in much of the non-Asian tropics. Until now, no endemic locality, as confirmed by regenerating outdoor populations, was known. A termite survey of the northern coastal desert of Chile and the vicinity of Lima, Peru, yielded 61 outdoor populations of C. brevis taken from 23 different native and exotic species of host woods at 19 localities. We review the taxonomic and biogeographic history of C. brevis and suggest climatic and biological factors that favor or limit C. brevis distribution. We also propose a scenario implicating a post-Colombian release of C. brevis by shipboard infestations and the movement of infested wood during the early Spanish Empire to the present time.

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Abstract:Of the more than 2,300 tennite species in the world, 183 species are known to damage buildings and 83 species cause significant damage. Subterranean tennites, including mound building and arboreal species, account for 147 (80%) of the economically important species. The genus Coptotermes contains the largest number of pest species (28), whereas the genus Cryptotermes, especially Cr. brevis, is the most widely introduced. The world-wide economic impact figure of tennites is uncertain, but the control cost for tennite pests in the United States was estimated at $1.5 billion annually in 1994. Because of differences in their life histories, control measures differ between subterranean and drywood species. Insecticide barriers are used for exclusion of soil-borne subterranean tennites, whereas slow-acting baits are used for population control of subterranean tennite colonies in and near structures. Whole-structure treatments (fumigation and heat), compartmental treatments (heat or cold), and local treatments (wood surface treatments or insecticide injection) are the primary tools for drywood tennite control.