Fidelity varies in the symbiosis between a gutless marine worm and its microbial consortium.
Animal-bacterial symbiosis
Intraspecific genetic variation
Microbiome
Phylosymbiosis
Symbiont transmission
Journal
Microbiome
ISSN: 2049-2618
Titre abrégé: Microbiome
Pays: England
ID NLM: 101615147
Informations de publication
Date de publication:
22 10 2022
22 10 2022
Historique:
received:
21
06
2022
accepted:
15
09
2022
entrez:
23
10
2022
pubmed:
24
10
2022
medline:
26
10
2022
Statut:
epublish
Résumé
Many animals live in intimate associations with a species-rich microbiome. A key factor in maintaining these beneficial associations is fidelity, defined as the stability of associations between hosts and their microbiota over multiple host generations. Fidelity has been well studied in terrestrial hosts, particularly insects, over longer macroevolutionary time. In contrast, little is known about fidelity in marine animals with species-rich microbiomes at short microevolutionary time scales, that is at the level of a single host population. Given that natural selection acts most directly on local populations, studies of microevolutionary partner fidelity are important for revealing the ecological and evolutionary processes that drive intimate beneficial associations within animal species. In this study on the obligate symbiosis between the gutless marine annelid Olavius algarvensis and its consortium of seven co-occurring bacterial symbionts, we show that partner fidelity varies across symbiont species from strict to absent over short microevolutionary time. Using a low-coverage sequencing approach that has not yet been applied to microbial community analyses, we analysed the metagenomes of 80 O. algarvensis individuals from the Mediterranean and compared host mitochondrial and symbiont phylogenies based on single-nucleotide polymorphisms across genomes. Fidelity was highest for the two chemoautotrophic, sulphur-oxidizing symbionts that dominated the microbial consortium of all O. algarvensis individuals. In contrast, fidelity was only intermediate to absent in the sulphate-reducing and spirochaetal symbionts with lower abundance. These differences in fidelity are likely driven by both selective and stochastic forces acting on the consistency with which symbionts are vertically transmitted. We hypothesize that variable degrees of fidelity are advantageous for O. algarvensis by allowing the faithful transmission of their nutritionally most important symbionts and flexibility in the acquisition of other symbionts that promote ecological plasticity in the acquisition of environmental resources. Video Abstract.
Sections du résumé
BACKGROUND
Many animals live in intimate associations with a species-rich microbiome. A key factor in maintaining these beneficial associations is fidelity, defined as the stability of associations between hosts and their microbiota over multiple host generations. Fidelity has been well studied in terrestrial hosts, particularly insects, over longer macroevolutionary time. In contrast, little is known about fidelity in marine animals with species-rich microbiomes at short microevolutionary time scales, that is at the level of a single host population. Given that natural selection acts most directly on local populations, studies of microevolutionary partner fidelity are important for revealing the ecological and evolutionary processes that drive intimate beneficial associations within animal species.
RESULTS
In this study on the obligate symbiosis between the gutless marine annelid Olavius algarvensis and its consortium of seven co-occurring bacterial symbionts, we show that partner fidelity varies across symbiont species from strict to absent over short microevolutionary time. Using a low-coverage sequencing approach that has not yet been applied to microbial community analyses, we analysed the metagenomes of 80 O. algarvensis individuals from the Mediterranean and compared host mitochondrial and symbiont phylogenies based on single-nucleotide polymorphisms across genomes. Fidelity was highest for the two chemoautotrophic, sulphur-oxidizing symbionts that dominated the microbial consortium of all O. algarvensis individuals. In contrast, fidelity was only intermediate to absent in the sulphate-reducing and spirochaetal symbionts with lower abundance. These differences in fidelity are likely driven by both selective and stochastic forces acting on the consistency with which symbionts are vertically transmitted.
CONCLUSIONS
We hypothesize that variable degrees of fidelity are advantageous for O. algarvensis by allowing the faithful transmission of their nutritionally most important symbionts and flexibility in the acquisition of other symbionts that promote ecological plasticity in the acquisition of environmental resources. Video Abstract.
Identifiants
pubmed: 36273146
doi: 10.1186/s40168-022-01372-2
pii: 10.1186/s40168-022-01372-2
pmc: PMC9587655
doi:
Substances chimiques
Sulfates
0
Sulfur
70FD1KFU70
Types de publication
Video-Audio Media
Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
178Informations de copyright
© 2022. The Author(s).
Références
Genome Res. 2015 Jun;25(6):918-25
pubmed: 25883319
Front Genet. 2021 May 10;12:648229
pubmed: 34040632
Bioinformatics. 2015 Oct 15;31(20):3350-2
pubmed: 26099265
BMC Genomics. 2013;14 Suppl 1:S7
pubmed: 23368723
Cell Microbiol. 2012 Mar;14(3):334-42
pubmed: 22168434
Bioinformatics. 2006 Jul 1;22(13):1658-9
pubmed: 16731699
Proc Biol Sci. 2009 Aug 22;276(1669):2963-9
pubmed: 19474039
mBio. 2016 Mar 31;7(2):e02099
pubmed: 27034285
PLoS One. 2012;7(12):e52249
pubmed: 23284954
Nat Commun. 2018 Nov 22;9(1):4921
pubmed: 30467310
Proc Biol Sci. 2019 Feb 13;286(1896):20181281
pubmed: 30887877
Appl Environ Microbiol. 2006 Aug;72(8):5527-36
pubmed: 16885306
Proc Biol Sci. 2000 Dec 22;267(1461):2517-21
pubmed: 11197128
Environ Microbiol. 2015 Dec;17(12):5023-35
pubmed: 26013766
ISME J. 2021 Jan;15(1):141-153
pubmed: 32934356
Nat Rev Microbiol. 2008 Oct;6(10):725-40
pubmed: 18794911
Genome Res. 2016 Nov;26(11):1612-1625
pubmed: 27803195
mSystems. 2018 Dec 18;3(6):
pubmed: 30574559
Nat Commun. 2021 Aug 26;12(1):5141
pubmed: 34446709
Proc Biol Sci. 2020 Sep 9;287(1934):20200820
pubmed: 32873208
Trends Microbiol. 2017 May;25(5):375-390
pubmed: 28336178
Nat Commun. 2018 Nov 30;9(1):5114
pubmed: 30504855
Science. 2008 Jun 20;320(5883):1647-51
pubmed: 18497261
ISME J. 2022 Sep;16(9):2132-2143
pubmed: 35715703
mSphere. 2020 Aug 26;5(4):
pubmed: 32848005
Mol Biol Evol. 2013 Apr;30(4):772-80
pubmed: 23329690
Curr Biol. 2020 May 18;30(10):1949-1957.e6
pubmed: 32243856
Nat Rev Microbiol. 2010 Mar;8(3):218-30
pubmed: 20157340
Nature. 2006 Oct 26;443(7114):950-5
pubmed: 16980956
Nat Ecol Evol. 2022 Jan;6(1):77-87
pubmed: 34949814
Philos Trans R Soc Lond B Biol Sci. 2011 May 12;366(1569):1389-400
pubmed: 21444313
Environ Microbiol. 2018 Aug 22;:
pubmed: 30136358
Appl Environ Microbiol. 2005 Mar;71(3):1553-61
pubmed: 15746360
Mol Biol Evol. 2015 Oct;32(10):2798-800
pubmed: 26130081
PLoS Biol. 2016 Nov 18;14(11):e2000225
pubmed: 27861590
Mol Phylogenet Evol. 2013 Nov;69(2):313-9
pubmed: 22982435
Front Microbiol. 2014 Oct 17;5:532
pubmed: 25368606
Genome Res. 2010 Sep;20(9):1297-303
pubmed: 20644199
Bioinformatics. 2014 Aug 1;30(15):2114-20
pubmed: 24695404
Nat Biotechnol. 2016 May;34(5):525-7
pubmed: 27043002
Bioinformatics. 2014 May 1;30(9):1312-3
pubmed: 24451623
Int J Syst Evol Microbiol. 2014 Feb;64(Pt 2):346-351
pubmed: 24505072
Proc Natl Acad Sci U S A. 2006 Aug 22;103(34):12803-6
pubmed: 16908834
Nature. 1995 Nov 30;378(6556):489-92
pubmed: 7477404
Environ Microbiol. 2008 Dec;10(12):3404-16
pubmed: 18764872
mSystems. 2021 Apr 6;6(2):
pubmed: 33824199
Philos Trans R Soc Lond B Biol Sci. 2020 Sep 28;375(1808):20190590
pubmed: 32772675
Mol Ecol. 2017 Oct;26(20):5369-5406
pubmed: 28746784
Nat Rev Genet. 2003 Jun;4(6):457-69
pubmed: 12776215
Cell Host Microbe. 2021 Jul 14;29(7):1167-1176.e9
pubmed: 34111423
Integr Comp Biol. 2002 Apr;42(2):369-80
pubmed: 21708730
Microbiol Resour Announc. 2020 Apr 16;9(16):
pubmed: 32299882
J Theor Biol. 1991 Mar 7;149(1):63-74
pubmed: 1881147
Nat Commun. 2017 Jul 04;8:15973
pubmed: 28675159
Appl Environ Microbiol. 2020 Mar 18;86(7):
pubmed: 31953337
Appl Environ Microbiol. 2014 Dec;80(23):7378-87
pubmed: 25239900
Nat Ecol Evol. 2019 Aug;3(8):1172-1183
pubmed: 31285574
ISME J. 2020 Jun;14(6):1584-1599
pubmed: 32203121
Proc Natl Acad Sci U S A. 2011 Jun 28;108 Suppl 2:10800-7
pubmed: 21690339
Nat Microbiol. 2019 Dec;4(12):2487-2497
pubmed: 31611646
Nucleic Acids Res. 2013 Jan;41(Database issue):D590-6
pubmed: 23193283
Nat Commun. 2017 Feb 23;8:14319
pubmed: 28230052
Methods. 2016 Jun 1;102:3-11
pubmed: 27012178
mBio. 2018 Sep 11;9(5):
pubmed: 30206171
G3 (Bethesda). 2018 Jan 4;8(1):79-89
pubmed: 29118030
Microbiol Resour Announc. 2020 Jul 30;9(31):
pubmed: 32732238
Proc Natl Acad Sci U S A. 2018 Jun 12;115(24):E5576-E5584
pubmed: 29844191
mSystems. 2020 Oct 27;5(5):
pubmed: 33109753
Appl Environ Microbiol. 2011 Dec;77(23):8400-8
pubmed: 21948847
Proc Natl Acad Sci U S A. 2015 Aug 18;112(33):10169-76
pubmed: 25713367
BMC Genomics. 2016 Nov 21;17(1):942
pubmed: 27871231
Nat Commun. 2016 Jun 16;7:11870
pubmed: 27306690
Sci Rep. 2016 Dec 09;6:38770
pubmed: 27934910
Mol Ecol. 2018 Apr;27(8):2039-2056
pubmed: 29215202
J Comput Biol. 2012 May;19(5):455-77
pubmed: 22506599
Appl Environ Microbiol. 2018 Mar 19;84(7):
pubmed: 29330187
Nature. 2001 May 17;411(6835):298-302
pubmed: 11357130
mSystems. 2020 Jan 14;5(1):
pubmed: 31937678
Nat Rev Microbiol. 2020 Sep;18(9):491-506
pubmed: 32499497
Nat Ecol Evol. 2022 Jun;6(6):750-762
pubmed: 35393600
Bioinformatics. 2013 Apr 15;29(8):1072-5
pubmed: 23422339
Genome Res. 2015 Jul;25(7):1043-55
pubmed: 25977477
Cell Host Microbe. 2018 Jul 11;24(1):133-145.e5
pubmed: 30001516
ISME J. 2021 Oct;15(10):2956-2968
pubmed: 33941888
Annu Rev Genet. 2008;42:165-90
pubmed: 18983256
mSystems. 2017 Jan 17;2(1):
pubmed: 28144631
BMC Bioinformatics. 2014 Nov 25;15:356
pubmed: 25420514
Appl Environ Microbiol. 2003 Apr;69(4):2058-64
pubmed: 12676683
Mol Ecol. 2016 Jul;25(13):3203-23
pubmed: 26826340
ISME J. 2020 Jan;14(1):259-273
pubmed: 31624345
J Anim Ecol. 2018 Mar;87(2):323-330
pubmed: 28502120
Proc Natl Acad Sci U S A. 2012 May 8;109(19):E1173-82
pubmed: 22517752
ISME J. 2020 Sep;14(9):2211-2222
pubmed: 32444811
Mol Mar Biol Biotechnol. 1994 Oct;3(5):294-9
pubmed: 7881515
Environ Microbiol. 2008 Mar;10(3):727-37
pubmed: 18237306
Nucleic Acids Res. 2013 Jul;41(13):e129
pubmed: 23661685
ISME J. 2017 Jun;11(6):1359-1371
pubmed: 28234348
Bioinformatics. 2009 Aug 15;25(16):2078-9
pubmed: 19505943
Proc Biol Sci. 2020 Mar 11;287(1922):20192900
pubmed: 32126958
Heredity (Edinb). 2018 Dec;121(6):524-536
pubmed: 29453423
Mol Ecol. 2000 Oct;9(10):1657-9
pubmed: 11050560
Mol Biol Evol. 2008 Apr;25(4):673-87
pubmed: 18192696
Proc Biol Sci. 2010 Oct 22;277(1697):3055-64
pubmed: 20573624
Proc Biol Sci. 2015 Apr 7;282(1804):20142957
pubmed: 25740892
Environ Microbiol. 2021 Apr;23(4):2184-2198
pubmed: 33415800
FEMS Microbiol Lett. 2019 Feb 1;366(3):
pubmed: 30649338
Bioinformatics. 2014 May 15;30(10):1486-7
pubmed: 24458950
Microbiome. 2018 Oct 10;6(1):181
pubmed: 30305166
PLoS Genet. 2020 Aug 25;16(8):e1008935
pubmed: 32841233
PeerJ. 2015 Aug 27;3:e1165
pubmed: 26336640
Environ Microbiol. 2009 Aug;11(8):2136-47
pubmed: 19397674
Nature. 2017 Aug 2;548(7665):43-51
pubmed: 28770836
PLoS One. 2012;7(7):e37558
pubmed: 22911679
Bioinformatics. 2018 Jul 15;34(14):2371-2375
pubmed: 29506021