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...

Full description

Bibliographic Details
Main Authors: Peter eMøller, Marie Braad Lund, Andreas eSchramm
Format: Article
Language:English
Published: Frontiers Media S.A. 2015-05-01
Series:Frontiers in Microbiology
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fmicb.2015.00529/full
_version_ 1811303905585266688
author Peter eMøller
Marie Braad Lund
Andreas eSchramm
author_facet Peter eMøller
Marie Braad Lund
Andreas eSchramm
author_sort Peter eMøller
collection DOAJ
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.
first_indexed 2024-04-13T07:56:27Z
format Article
id doaj.art-00037d5811484837a8aab9fcb483d941
institution Directory Open Access Journal
issn 1664-302X
language English
last_indexed 2024-04-13T07:56:27Z
publishDate 2015-05-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Microbiology
spelling doaj.art-00037d5811484837a8aab9fcb483d9412022-12-22T02:55:23ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2015-05-01610.3389/fmicb.2015.00529144493Evolution of the tripartite symbiosis between earthworms, Verminephrobacter and Flexibacter-like bacteriaPeter eMøller0Marie Braad Lund1Andreas eSchramm2Section for Microbiology, Aarhus UniversityAarhus Institute of Advanced Studies (AIAS), Aarhus UniversitySection for Microbiology, Aarhus UniversityNephridial (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.http://journal.frontiersin.org/Journal/10.3389/fmicb.2015.00529/fullSymbiosisCo-EvolutionEarthwormverminephrobacternephridiaCo-speciation
spellingShingle Peter eMøller
Marie Braad Lund
Andreas eSchramm
Evolution of the tripartite symbiosis between earthworms, Verminephrobacter and Flexibacter-like bacteria
Frontiers in Microbiology
Symbiosis
Co-Evolution
Earthworm
verminephrobacter
nephridia
Co-speciation
title 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_short 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
topic Symbiosis
Co-Evolution
Earthworm
verminephrobacter
nephridia
Co-speciation
url http://journal.frontiersin.org/Journal/10.3389/fmicb.2015.00529/full
work_keys_str_mv AT peteremøller evolutionofthetripartitesymbiosisbetweenearthwormsverminephrobacterandflexibacterlikebacteria
AT mariebraadlund evolutionofthetripartitesymbiosisbetweenearthwormsverminephrobacterandflexibacterlikebacteria
AT andreaseschramm evolutionofthetripartitesymbiosisbetweenearthwormsverminephrobacterandflexibacterlikebacteria