Evolution of the tripartite symbiosis between earthworms, Verminephrobacter and Flexibacter-like bacteria

Nephridial (excretory organ) symbionts are widespread in lumbricid earthworms and the complexity of the nephridial symbiont communities varies greatly between earthworm species. The two most common symbionts are the well-described Verminephrobacter and less well-known Flexibacter-like bacteria. Verm...

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Main Authors:	Møller, Peter, Lund, Marie B., Schramm, Andreas
Format:	Online
Language:	English
Published:	Frontiers Media S.A. 2015
Online Access:	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4445045/

id	pubmed-4445045
recordtype	oai_dc
spelling	pubmed-44450452015-06-12 Evolution of the tripartite symbiosis between earthworms, Verminephrobacter and Flexibacter-like bacteria Møller, Peter Lund, Marie B. Schramm, Andreas Microbiology Nephridial (excretory organ) symbionts are widespread in lumbricid earthworms and the complexity of the nephridial symbiont communities varies greatly between earthworm species. The two most common symbionts are the well-described Verminephrobacter and less well-known Flexibacter-like bacteria. Verminephrobacter are present in almost all lumbricid earthworms, they are species-specific, vertically transmitted, and have presumably been associated with their hosts since the origin of lumbricids. Flexibacter-like symbionts have been reported from about half the investigated earthworms; they are also vertically transmitted. To investigate the evolution of this tri-partite symbiosis, phylogenies for 18 lumbricid earthworm species were constructed based on two mitochondrial genes, NADH dehydrogenase subunit 2 (ND2) and cytochrome c oxidase subunit I (COI), and compared to their symbiont phylogenies based on RNA polymerase subunit B (rpoB) and 16S rRNA genes. The two nephridial symbionts showed markedly different evolutionary histories with their hosts. For Verminephrobacter, clear signs of long-term host-symbiont co-evolution with rare host switching events confirmed its ancient association with lumbricid earthworms, likely dating back to their last common ancestor about 100 million years (MY) ago. In contrast, phylogenies for the Flexibacter-like symbionts suggested an ability to switch to new hosts, to which they adapted and subsequently became species-specific. Putative co-speciation events were only observed with closely related host species; on that basis, this secondary symbiosis was estimated to be minimum 45 MY old. Based on the monophyletic clustering of the Flexibacter-like symbionts, the low 16S rRNA gene sequence similarity to the nearest described species (<92%) and environmental sequences (<94.2%), and the specific habitat in the earthworm nephridia, we propose a new candidate genus for this group, Candidatus Nephrothrix. Frontiers Media S.A. 2015-05-27 /pmc/articles/PMC4445045/ /pubmed/26074907 http://dx.doi.org/10.3389/fmicb.2015.00529 Text en Copyright © 2015 Møller, Lund and Schramm. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
repository_type	Open Access Journal
institution_category	Foreign Institution
institution	US National Center for Biotechnology Information
building	NCBI PubMed
collection	Online Access
language	English
format	Online
author	Møller, Peter Lund, Marie B. Schramm, Andreas
spellingShingle	Møller, Peter Lund, Marie B. Schramm, Andreas Evolution of the tripartite symbiosis between earthworms, Verminephrobacter and Flexibacter-like bacteria
author_facet	Møller, Peter Lund, Marie B. Schramm, Andreas
author_sort	Møller, Peter
title	Evolution of the tripartite symbiosis between earthworms, Verminephrobacter and Flexibacter-like bacteria
title_short	Evolution of the tripartite symbiosis between earthworms, Verminephrobacter and Flexibacter-like bacteria
title_full	Evolution of the tripartite symbiosis between earthworms, Verminephrobacter and Flexibacter-like bacteria
title_fullStr	Evolution of the tripartite symbiosis between earthworms, Verminephrobacter and Flexibacter-like bacteria
title_full_unstemmed	Evolution of the tripartite symbiosis between earthworms, Verminephrobacter and Flexibacter-like bacteria
title_sort	evolution of the tripartite symbiosis between earthworms, verminephrobacter and flexibacter-like bacteria
description	Nephridial (excretory organ) symbionts are widespread in lumbricid earthworms and the complexity of the nephridial symbiont communities varies greatly between earthworm species. The two most common symbionts are the well-described Verminephrobacter and less well-known Flexibacter-like bacteria. Verminephrobacter are present in almost all lumbricid earthworms, they are species-specific, vertically transmitted, and have presumably been associated with their hosts since the origin of lumbricids. Flexibacter-like symbionts have been reported from about half the investigated earthworms; they are also vertically transmitted. To investigate the evolution of this tri-partite symbiosis, phylogenies for 18 lumbricid earthworm species were constructed based on two mitochondrial genes, NADH dehydrogenase subunit 2 (ND2) and cytochrome c oxidase subunit I (COI), and compared to their symbiont phylogenies based on RNA polymerase subunit B (rpoB) and 16S rRNA genes. The two nephridial symbionts showed markedly different evolutionary histories with their hosts. For Verminephrobacter, clear signs of long-term host-symbiont co-evolution with rare host switching events confirmed its ancient association with lumbricid earthworms, likely dating back to their last common ancestor about 100 million years (MY) ago. In contrast, phylogenies for the Flexibacter-like symbionts suggested an ability to switch to new hosts, to which they adapted and subsequently became species-specific. Putative co-speciation events were only observed with closely related host species; on that basis, this secondary symbiosis was estimated to be minimum 45 MY old. Based on the monophyletic clustering of the Flexibacter-like symbionts, the low 16S rRNA gene sequence similarity to the nearest described species (<92%) and environmental sequences (<94.2%), and the specific habitat in the earthworm nephridia, we propose a new candidate genus for this group, Candidatus Nephrothrix.
publisher	Frontiers Media S.A.
publishDate	2015
url	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4445045/
_version_	1613228047835594752

Evolution of the tripartite symbiosis between earthworms, Verminephrobacter and Flexibacter-like bacteria

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