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

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.

SUBMITTER: Noda S

PROVIDER: S-EPMC2717939 | biostudies-literature | 2009

REPOSITORIES: biostudies-literature

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

Noda Satoko S Hongoh Yuichi Y Sato Tomoyuki T Ohkuma Moriya M

BMC evolutionary biology 20090709

<h4>Background</h4>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 ...[more]

PMID: 19586555

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Project description:BACKGROUND:Diverse animals are intimately associated with microbial symbionts. How such host-symbiont associations have evolved is a fundamental biological issue. Recent studies have revealed a variety of evolutionary relationships, such as obligatory, facultative, and free-living, of gut bacterial symbiosis within the stinkbug family Pentatomidae, although the whole evolutionary picture remains elusive. RESULTS:Here we investigated a comprehensive assembly of Japanese pentatomid stinkbugs representing 28 genera, 35 species, and 143 populations. Polymerase chain reaction (PCR), cloning, and sequencing of bacterial 16S rRNA gene from their midgut symbiotic organ consistently detected a single bacterial species from each of the insect samples, indicating a general tendency toward monosymbiotic gut association. Bacterial sequences detected from different populations of the same species were completely or nearly identical, indicating that the majority of the gut symbiotic associations are stably maintained at the species level. Furthermore, bacterial sequences detected from different species in the same genus tended to form well-supported clades, suggesting that host-symbiont associations are often stable even at the genus level. Meanwhile, when we compared such sequences with published sequences available in DNA databases, we found a number of counter-examples to such stable host-symbiont relationships; i.e., symbionts from different host species in the same genus may be phylogenetically distant, and symbionts from the same host species may be phylogenetically diverse. Likewise, symbionts of diverse pentatomid species may be closely related to symbionts of other stinkbug families, and symbionts of diverse pentatomid species may even be allied to free-living bacteria. Molecular evolutionary analyses revealed that higher molecular evolutionary rates, higher AT nucleotide compositions, and smaller genome sizes tended to be associated with the pentatomid symbionts constituting the stable lineages, whereas these traits were rarely observed in the pentatomid symbionts of promiscuous type. CONCLUSIONS:These results indicate that gut symbiotic bacteria have evolved repeatedly and dynamically in the stinkbug family Pentatomidae, which have plausibly entailed frequent symbiont acquisitions, losses, replacements and transfers, while establishing a number of relatively stable host-symbiont associations. The diverse host-symbiont relationships observed in the Pentatomidae will provide an ideal arena for investigating the evolution of symbiosis experimentally and theoretically.

Dataset Information

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

Publications

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

Similar Datasets

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