Diversity and Evolution of Pigment Types in Marine Synechococcus Cyanobacteria.

cyanobacteria genomic island lateral gene transfer phycobiliprotein phycobilisome tycheposon

Journal

Genome biology and evolution
ISSN: 1759-6653
Titre abrégé: Genome Biol Evol
Pays: England
ID NLM: 101509707

Informations de publication

Date de publication:
10 04 2022
Historique:
accepted: 07 03 2022
pubmed: 12 3 2022
medline: 13 4 2022
entrez: 11 3 2022
Statut: ppublish

Résumé

Synechococcus cyanobacteria are ubiquitous and abundant in the marine environment and contribute to an estimated 16% of the ocean net primary productivity. Their light-harvesting complexes, called phycobilisomes (PBS), are composed of a conserved allophycocyanin core, from which radiates six to eight rods with variable phycobiliprotein and chromophore content. This variability allows Synechococcus cells to optimally exploit the wide variety of spectral niches existing in marine ecosystems. Seven distinct pigment types or subtypes have been identified so far in this taxon based on the phycobiliprotein composition and/or the proportion of the different chromophores in PBS rods. Most genes involved in their biosynthesis and regulation are located in a dedicated genomic region called the PBS rod region. Here, we examine the variability of gene content and organization of this genomic region in a large set of sequenced isolates and natural populations of Synechococcus representative of all known pigment types. All regions start with a tRNA-PheGAA and some possess mobile elements for DNA integration and site-specific recombination, suggesting that their genomic variability relies in part on a "tycheposon"-like mechanism. Comparison of the phylogenies obtained for PBS and core genes revealed that the evolutionary history of PBS rod genes differs from the core genome and is characterized by the co-existence of different alleles and frequent allelic exchange. We propose a scenario for the evolution of the different pigment types and highlight the importance of incomplete lineage sorting in maintaining a wide diversity of pigment types in different Synechococcus lineages despite multiple speciation events.

Identifiants

pubmed: 35276007
pii: 6547267
doi: 10.1093/gbe/evac035
pmc: PMC8995045
pii:
doi:

Substances chimiques

Phycobiliproteins 0
Phycobilisomes 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© The Author(s) 2022. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.

Références

Appl Environ Microbiol. 2001 Feb;67(2):991-4
pubmed: 11157276
J Biol Chem. 1992 Aug 15;267(23):16138-45
pubmed: 1644801
Environ Microbiol. 2020 May;22(5):1801-1815
pubmed: 31840403
Trends Ecol Evol. 2009 Jun;24(6):332-40
pubmed: 19307040
J Biol Chem. 1993 Jan 15;268(2):1226-35
pubmed: 8419325
J Biol Chem. 1992 Aug 15;267(23):16146-54
pubmed: 1644802
PLoS Genet. 2015 Feb 06;11(2):e1004941
pubmed: 25659072
Proc Natl Acad Sci U S A. 2012 Dec 4;109(49):20136-41
pubmed: 23161909
Photosynth Res. 2005;85(1):15-32
pubmed: 15977057
Bioinformatics. 2011 Feb 15;27(4):578-9
pubmed: 21149342
Bioinformatics. 2009 Jun 1;25(11):1422-3
pubmed: 19304878
Mol Biol Evol. 2013 Apr;30(4):772-80
pubmed: 23329690
Nucleic Acids Res. 2021 Jan 8;49(D1):D667-D676
pubmed: 33125079
Front Microbiol. 2020 Sep 15;11:567431
pubmed: 33042072
Annu Rev Microbiol. 2019 Sep 8;73:407-433
pubmed: 31500538
Microb Ecol. 2018 Jan;75(1):10-21
pubmed: 28667427
Proc Natl Acad Sci U S A. 2019 Mar 26;116(13):6457-6462
pubmed: 30846551
Front Microbiol. 2017 Jun 21;8:1151
pubmed: 28680419
J Bacteriol. 2004 Nov;186(21):7420-8
pubmed: 15489454
J Biol Chem. 1982 Apr 10;257(7):3429-33
pubmed: 6801045
Nat Rev Microbiol. 2014 Dec;12(12):841-50
pubmed: 25220308
Bioinformatics. 2014 May 1;30(9):1312-3
pubmed: 24451623
Mol Biol Evol. 2016 Jun;33(6):1635-8
pubmed: 26921390
Science. 1984 Apr 6;224(4644):80-3
pubmed: 17783529
Sci Data. 2018 Sep 04;5:180154
pubmed: 30179231
Front Microbiol. 2017 Feb 21;8:243
pubmed: 28270800
Front Microbiol. 2017 Jul 06;8:1254
pubmed: 28729864
Science. 2014 Apr 25;344(6182):416-20
pubmed: 24763590
Nat Ecol Evol. 2021 Jan;5(1):55-66
pubmed: 33168993
Proc Natl Acad Sci U S A. 2010 Jun 22;107(25):11453-8
pubmed: 20534528
Syst Biol. 2013 Nov;62(6):901-12
pubmed: 23925510
Mol Microbiol. 2008 Apr;68(2):263-76
pubmed: 18284595
Science. 2007 Aug 24;317(5841):1093-6
pubmed: 17717188
ISME J. 2019 Jul;13(7):1676-1687
pubmed: 30820035
Proc Natl Acad Sci U S A. 2016 Jun 14;113(24):E3365-74
pubmed: 27302952
Nucleic Acids Res. 2013 Jan;41(Database issue):D396-401
pubmed: 23175607
J Biol Chem. 2021 Jan-Jun;296:100031
pubmed: 33154169
Proc Natl Acad Sci U S A. 2021 Mar 16;118(11):
pubmed: 33707213
Annu Rev Biochem. 2006;75:567-605
pubmed: 16756503
ISME J. 2014 Sep;8(9):1892-903
pubmed: 24621524
Genetics. 1983 Oct;105(2):437-60
pubmed: 6628982
BMC Biol. 2010 May 25;8:70
pubmed: 20500830
Bioinformatics. 2011 Nov 1;27(21):2957-63
pubmed: 21903629
Environ Microbiol. 2019 May;21(5):1677-1686
pubmed: 30724442
Environ Microbiol. 2008 Jan;10(1):147-61
pubmed: 17900271
Biochim Biophys Acta Bioenerg. 2019 Jul 1;1860(7):549-561
pubmed: 31173730
Proc Natl Acad Sci U S A. 2018 Feb 27;115(9):E2010-E2019
pubmed: 29440402
Genome Biol Evol. 2012;4(4):443-56
pubmed: 22357598
Genome Biol. 2007;8(12):R259
pubmed: 18062815
Syst Biol. 2003 Oct;52(5):696-704
pubmed: 14530136
Environ Microbiol. 2017 Jan;19(1):142-158
pubmed: 27668842
Philos Trans R Soc Lond B Biol Sci. 2008 Dec 27;363(1512):4023-9
pubmed: 18852109
PLoS One. 2013 Oct 17;8(10):e77033
pubmed: 24146954
J Bacteriol. 2005 Mar;187(5):1685-94
pubmed: 15716439
Environ Microbiol. 2008 Jan;10(1):174-88
pubmed: 17903216
Genome Biol. 2008;9(5):R90
pubmed: 18507822
FEMS Microbiol Ecol. 2009 Sep;69(3):439-48
pubmed: 19624741
Bioinformatics. 2009 Aug 1;25(15):1972-3
pubmed: 19505945
ISME J. 2012 Feb;6(2):285-97
pubmed: 21955990
Trends Microbiol. 2007 Mar;15(3):135-41
pubmed: 17289390
FEMS Microbiol Ecol. 2014 May;88(2):231-49
pubmed: 24862161
J Bacteriol. 2006 May;188(9):3345-56
pubmed: 16621829
Front Microbiol. 2012 Jun 19;3:213
pubmed: 22723796
Mol Phylogenet Evol. 2012 Sep;64(3):381-92
pubmed: 22588203
J Mol Biol. 1995 Apr 21;248(1):79-96
pubmed: 7731046
Environ Microbiol. 2012 Feb;14(2):372-86
pubmed: 21651684
Proc Natl Acad Sci U S A. 2013 Jun 11;110(24):9824-9
pubmed: 23703908
PLoS One. 2013 Dec 31;8(12):e84459
pubmed: 24391958
ISME J. 2016 Feb;10(2):333-45
pubmed: 26208139
Adv Exp Med Biol. 2010;675:211-28
pubmed: 20532743
J Biol Chem. 2009 Apr 3;284(14):9290-8
pubmed: 19182270
Nature. 2016 Apr 28;532(7600):465-470
pubmed: 26863193
Front Microbiol. 2019 Jan 30;10:45
pubmed: 30761097
Proc Natl Acad Sci U S A. 2016 May 24;113(21):6077-82
pubmed: 27152022
Biochemistry. 2012 May 29;51(21):4271-9
pubmed: 22574919
Proc Natl Acad Sci U S A. 2017 Jul 3;114(27):E5424-E5433
pubmed: 28630351
Proc Natl Acad Sci U S A. 2021 Mar 2;118(9):
pubmed: 33627406

Auteurs

Théophile Grébert (T)

Sorbonne Université, Centre National de la Recherche Scientifique, UMR 7144 Adaptation and Diversity in the Marine Environment, Station Biologique, Roscoff 29680, France.

Laurence Garczarek (L)

Sorbonne Université, Centre National de la Recherche Scientifique, UMR 7144 Adaptation and Diversity in the Marine Environment, Station Biologique, Roscoff 29680, France.

Vincent Daubin (V)

UMR 5558 Biometry and Evolutionary Biology, Université Lyon 1, Villeurbanne 69622, France.

Florian Humily (F)

Sorbonne Université, Centre National de la Recherche Scientifique, UMR 7144 Adaptation and Diversity in the Marine Environment, Station Biologique, Roscoff 29680, France.

Dominique Marie (D)

Sorbonne Université, Centre National de la Recherche Scientifique, UMR 7144 Adaptation and Diversity in the Marine Environment, Station Biologique, Roscoff 29680, France.

Morgane Ratin (M)

Sorbonne Université, Centre National de la Recherche Scientifique, UMR 7144 Adaptation and Diversity in the Marine Environment, Station Biologique, Roscoff 29680, France.

Alban Devailly (A)

Sorbonne Université, Centre National de la Recherche Scientifique, UMR 7144 Adaptation and Diversity in the Marine Environment, Station Biologique, Roscoff 29680, France.

Gregory K Farrant (GK)

Sorbonne Université, Centre National de la Recherche Scientifique, UMR 7144 Adaptation and Diversity in the Marine Environment, Station Biologique, Roscoff 29680, France.

Isabelle Mary (I)

CNRS, Laboratoire Microorganismes: Génome et Environnement, Université Clermont Auvergne, Clermont-Ferrand 63000, France.

Daniella Mella-Flores (D)

Sorbonne Université, Centre National de la Recherche Scientifique, UMR 7144 Adaptation and Diversity in the Marine Environment, Station Biologique, Roscoff 29680, France.

Gwenn Tanguy (G)

Centre National de la Recherche Scientifique, FR 2424, Station Biologique, Roscoff 29680, France.

Karine Labadie (K)

Genoscope, Institut de biologie François-Jacob, Commissariat à l'Énergie Atomique (CEA), Université Paris-Saclay, Evry, France.

Patrick Wincker (P)

Génomique Métabolique, Genoscope, Institut de biologie François Jacob, CEA, CNRS, Université d'Evry, Université Paris-Saclay, Evry, France.

David M Kehoe (DM)

Department of Biology, Indiana University, Bloomington, Indiana 47405.

Frédéric Partensky (F)

Sorbonne Université, Centre National de la Recherche Scientifique, UMR 7144 Adaptation and Diversity in the Marine Environment, Station Biologique, Roscoff 29680, France.

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Classifications MeSH