Microhabitat-specificity of the hindgut microbiota in higher termites

Termites are a group of eusocial insects in the superorder Dietyaptera, believed to have evolved from a lineage of ancient cockroach-like ancestors 150 million years ago. They play an important role in the breakdown of dead plant material, with the help of microorganisms harboured in the gut. Th...

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1. Verfasser: Mikaelyan, Aram
Beteiligte: Brune, Andreas (Prof. Dr.) (BetreuerIn (Doktorarbeit))
Format: Dissertation
Sprache:Englisch
Veröffentlicht: Philipps-Universität Marburg 2013
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Zusammenfassung:Termites are a group of eusocial insects in the superorder Dietyaptera, believed to have evolved from a lineage of ancient cockroach-like ancestors 150 million years ago. They play an important role in the breakdown of dead plant material, with the help of microorganisms harboured in the gut. The termites can be classified into flagellate-harbouring lower termites and flagellate-free higher termites. In comparison to the lower termites, the higher termites have undergone immense phylogenetic and dietary diversification, that has led to major changes in their gut structure. This diversification in the host is reflected in differences in their gut communities. To understand how host phylogeny and diet help shape bacterial communities in higher termites, I conducted an extensive pyrosequencingbased community survey of the gut communities of the major higher termite subfamilies, Macrotermitinae, Termitinae, and Nasutitermitinae. First, I constructed clone libraries and calculated phylogenetic trees for relevant bacterial taxa found in a variety of higher termites. The node information in these trees was used to provide a robust phylogenetic backbone for the accurate taxonomic assignment of the shorter pyrosequences. The analysis revealed that phylogenetically related termites in general, have similar community structure. However, one of the wood-feeding termites showed a greater similarity in gut community structure to other wood-feeders, in spite of not being phylogenetically related to them. The results suggest that although host phylogeny appears to be the major driving force in the determination of gut community membership, host diet can significantly contribute to community structure. However, far from being a homogenous environment, the higher termite gut is a highly structured habitat and shows the presence of spatially separated and physicochemically distinct compartments. Conditions unique to each compartment, playa significant role in shaping distinct compartment-specific communities. I used pyrotag sequencing to conduct an in-depth analysis of the communities of gut compartments from termites belonging to the families Termitinae and Nasutitermitinae. I found that homologous compartments from closely related termites are more similar in their community structure than adjacent compartments from the same termite. Based on our results, we hypothesize that similar ecological conditions such as increased alkalinity in the anterior gut, drive community structure in the gut compartments, and are reflected in overall hindgut community structure as well. The paunch (or P3 compartment) is the most voluminous of all hindgut compartments in wood-feeding higher termites, and is densely colonized by bacteria. Studies have shown that cellulase activity in the hindgut is particle-associated and possibly of bacterial origin. By fractionation of particles in the paunch lumen, using density-dependent centrifugation , I was able to show that the fraction enriched in wood fibers contributes substantially to the total cellulase activity in the hindgut. Using pyrosequencing, I examined the bacterial communities associated with the wood fibers in two wood-feeding members of the Nasutitermitinae. The results revealed the presence of a distinct cellulolytic fiber-associated community, primarily composed of the phyla TG3, Fibrobacteres and Spirochaetes. This fiber-associated community appears to have filled the niche for cellulose digestion, vacated by the flagellates. Lastly, the gut wall in termites is one of the major habitats in the gut, and home to an endospore-forming filamentous bacterium called 'Candidatus Arthromitus'. Due to the lack of a cultured isolate, the phylogenetic identity of 'Arthromitus' was disputed, and often confused with similar filamentous bacteria from mammalian guts. Phylogenetic analysis of picked filaments reveals 'Candidatus Arthromitus' to be a diverse clade of bacteria, found widely among arthropods, that is distinct from the segmented filamentous sequences recovered from mammalian guts.
DOI:10.17192/z2013.0753