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

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 o...

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Autores principales: Noda, Satoko, Hongoh, Yuichi, Sato, Tomoyuki, Ohkuma, Moriya
Formato: Texto
Lenguaje:English
Publicado: BioMed Central 2009
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2717939/
https://www.ncbi.nlm.nih.gov/pubmed/19586555
http://dx.doi.org/10.1186/1471-2148-9-158
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author Noda, Satoko
Hongoh, Yuichi
Sato, Tomoyuki
Ohkuma, Moriya
author_facet Noda, Satoko
Hongoh, Yuichi
Sato, Tomoyuki
Ohkuma, Moriya
author_sort Noda, Satoko
collection PubMed
description 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.
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spelling pubmed-27179392009-07-30 Complex coevolutionary history of symbiotic Bacteroidales bacteria of various protists in the gut of termites Noda, Satoko Hongoh, Yuichi Sato, Tomoyuki Ohkuma, Moriya BMC Evol Biol Research Article 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. BioMed Central 2009-07-09 /pmc/articles/PMC2717939/ /pubmed/19586555 http://dx.doi.org/10.1186/1471-2148-9-158 Text en Copyright © 2009 Noda et al; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( (http://creativecommons.org/licenses/by/2.0) ), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Noda, Satoko
Hongoh, Yuichi
Sato, Tomoyuki
Ohkuma, Moriya
Complex coevolutionary history of symbiotic Bacteroidales bacteria of various protists in the gut of termites
title Complex coevolutionary history of symbiotic Bacteroidales bacteria of various protists in the gut of termites
title_full Complex coevolutionary history of symbiotic Bacteroidales bacteria of various protists in the gut of termites
title_fullStr Complex coevolutionary history of symbiotic Bacteroidales bacteria of various protists in the gut of termites
title_full_unstemmed Complex coevolutionary history of symbiotic Bacteroidales bacteria of various protists in the gut of termites
title_short Complex coevolutionary history of symbiotic Bacteroidales bacteria of various protists in the gut of termites
title_sort complex coevolutionary history of symbiotic bacteroidales bacteria of various protists in the gut of termites
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2717939/
https://www.ncbi.nlm.nih.gov/pubmed/19586555
http://dx.doi.org/10.1186/1471-2148-9-158
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