Ecological and evolutionary drivers of microbial community structure in termite guts

Presumably descending from subsocial cockroaches 150 million years ago, termites are an order of social insects that gained the ability to digest wood through the acquisition of cellulolytic flagellates. These eukaryotic protists fill up the bulk of the hindgut volume and are the major habitat of...

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Bibliographic Details
Main Author: Dietrich, Carsten
Contributors: Brune, Andreas (Prof. Dr.) (Thesis advisor)
Format: Dissertation
Language:English
Published: Philipps-Universität Marburg 2015
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Summary:Presumably descending from subsocial cockroaches 150 million years ago, termites are an order of social insects that gained the ability to digest wood through the acquisition of cellulolytic flagellates. These eukaryotic protists fill up the bulk of the hindgut volume and are the major habitat of the prokaryotic community present in the digestive tract of lower termites. The complete loss of gut flagellates in the youngest termite family Termitidae, also called higher termites, led to an entirely prokaryotic gut microbiota as well as a substantial dietary diversification and enormous ecological success. While the subfamily Macrotermitinae established a symbiosis with wood-degrading fungi of the genus Termitomyces, other higher termites exploit diets with a higher degree of humification. Previous studies on the gut communities of termites have observed that while the gut microbiota of closely related hosts is very similar, those of more distantly related hosts are characterized by considerable differences in gut communities. Since these observations are based on highly limited samplings of hosts, it is uncertain if these differences reflect important evolutionary patterns. This dissertation includes studies examining the archaeal and bacterial diversity of the gut microbiota over a wide range of termites using high-throughput sequencing of the 16S rRNA genes. In comparison to the rather simple archaeal communities, which were mainly composed of methanogens, the bacterial gut microbiota were characterized by considerably higher diversity. At the phylum-level, Bacteroidetes, Firmicutes, Proteobacteria and Spirochaetes were ubiquitously distributed among the termites, albeit with differences in relative abundance. Other phyla, however, such as Elusimicrobia, Fibrobacteres and the candidate division TG3, occured only in certain host groups of termites. The distribution pattern of archaeal and bacterial lineages reflects both host phylogeny and differences in the digestive strategy of the host. Although several genus-level bacterial lineages showed a certain degree of host-specificity, phylogenetic analyses of the amplified rRNA genes showed that these bacterial lineages do not appear to be cospeciating with their hosts. The findings of studies included in this dissertation and other published studies were evaluated to identify potential drivers of community structure and other shaping mechanisms. Thus, gut community structure in termites is primarily shaped by habitat and niche selection. The stochastic element of these mechanisms, however, is strongly attenuated by proctodeal trophallaxis, which facilitates coevolution and might ultimately lead to cospeciation. While coevolution is likely true for many lineages and documented by host-specific microbial lineages, there is only little evidence of cospeciation in the gut microbiota of termites. If present, it is restricted almost exclusively to flagellates and their symbionts in lower termites. The higher wood-feeding termites have long been associated with a marked abundance of the phyla Fibrobacteres and cand. div. TG3. Although these phyla have been shown to be members of a specific cellulolytic community associated with wood particles in the hindguts of higher termites, their full functional potential still remains unknown. In order to elucidate the role of these organisms, a study in this dissertation carries out metagenomic analyses of various higher termites. In wood-feeding representatives, Fibrobacteres and cand. div. TG3 were in fact highly abundant, but only a few or no genes could be assigned to both groups by the usual database-dependent classification programs due to the lack of suitable genomes in these databases. In response, a new study was conceived to compensate this discrepancy. By further development of a new reference-independent method, over 30 population genomes of Fibrobacteres and cand. div. TG3 could be reconstructed from the metagenomic data sets. Subsequent comparative analysis revealed that organisms of both groups differ in their potential of wood degradation, but likely complement each other. Further analyses indicate that representatives of both groups might be able to fix nitrogen and respire under hypoxic conditions — two favourable adaptations to the unique termite gut environment.
Physical Description:254 Pages
DOI:https://doi.org/10.17192/z2015.0344