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Open Access Research article

Complex coevolutionary history of symbiotic Bacteroidales bacteria of various protists in the gut of termites

Satoko Noda13, Yuichi Hongoh14, Tomoyuki Sato15 and Moriya Ohkuma12*

Author Affiliations

1 Ecomolecular Biorecycling Science Research Team, RIKEN Advanced Science Institute, Wako, Saitama 351-0198, Japan

2 Microbe Division/Japan Collection of Microorganisms, RIKEN Bioresource Center, Wako, Saitama 351-0198, Japan

3 Current address: Interdisciplinary Graduate School of Medicine and Engineering, University of Yamanashi, Yamanashi 400-8510, Japan

4 Current address: Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, Tokyo 152-8550, Japan

5 Current address: Research Institute of Genome-based Biofactory, Advanced Industrial Science and Technology (AIST), Hokkaido 062-8517, Japan

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BMC Evolutionary Biology 2009, 9:158  doi:10.1186/1471-2148-9-158

Published: 9 July 2009

Abstract

Background

The microbial community in the gut of termites is responsible for the efficient decomposition of recalcitrant lignocellulose. Prominent features of this community are its complexity and the associations of prokaryotes with the cells of cellulolytic flagellated protists. Bacteria in the order Bacteroidales are involved in associations with a wide variety of gut protist species as either intracellular endosymbionts or surface-attached ectosymbionts. In particular, ectosymbionts exhibit distinct morphological patterns of the associations. Therefore, these Bacteroidales symbionts provide an opportunity to investigate not only the coevolutionary relationships with the host protists and their morphological evolution but also how symbiotic associations between prokaryotes and eukaryotes occur and evolve within a complex symbiotic community.

Results

Molecular phylogeny of 31 taxa of Bacteroidales symbionts from 17 protist genera in 10 families was examined based on 16S rRNA gene sequences. Their localization, morphology, and specificity were also examined by fluorescent in situ hybridizations. Although a monophyletic grouping of the ectosymbionts occurred in three related protist families, the symbionts of different protist genera were usually dispersed among several phylogenetic clusters unique to termite-gut bacteria. Similar morphologies of the associations occurred in multiple lineages of the symbionts. Nevertheless, the symbionts of congeneric protist species were closely related to one another, and in most cases, each host species harbored a unique Bacteroidales species. The endosymbionts were distantly related to the ectosymbionts examined so far.

Conclusion

The coevolutionary history of gut protists and their associated Bacteroidales symbionts is complex. We suggest multiple independent acquisitions of the Bacteroidales symbionts by different protist genera from a pool of diverse bacteria in the gut community. In this sense, the gut could serve as a reservoir of diverse bacteria for associations with the protist cells. The similar morphologies are considered a result of evolutionary convergence. Despite the complicated evolutionary history, the host-symbiont relationships are mutually specific, suggesting their cospeciations at the protist genus level with only occasional replacements.