[en] Oxygenic photosynthesis, which converts solar energy into carbohydrates via a linear electron transport chain and two photosystems (PSII and PSI), first appeared in cyanobacteria approximately 3.3 Ga and drove the Great Oxidation Event around 2.4 Ga. During this period, euxinic conditions-characterized by sulfidic, anoxic oceans-posed a metabolic challenge to cyanobacteria, as sulfide inhibits PSII, the reaction center responsible for water splitting. Here, we report the presence of a sulfide-quinone reductase (SQR) enzyme in Antarctic representatives of Gloeobacterales, the earliest-branching cyanobacterial lineage. Phylogenetic analyses consistently position these SQR sequences at the base of the cyanobacterial clade, likely predating the multiple lateral transfers reported for this gene in the phylum. Additional searches in metagenomic data sets indicate that such sequences are restricted to cold environments. Our findings unveil possible adaptive strategies of early cyanobacteria to cope with sulfidic stress and point to Antarctic lakes as preserved natural laboratories for investigating cyanobacterial diversification and the evolution of oxygenic photosynthesis under euxinic conditions.IMPORTANCEThe diversification of cyanobacteria during and after the Great Oxidation Event occurred in early Proterozoic oceans that were partially euxinic (anoxic and sulfidic), a condition generally considered incompatible with oxygenic photosynthesis due to photosystem II inhibition. The presence of a sulfide quinone reductase in an early diverging cyanobacterium lacking thylakoids, isolated from Antarctica, suggests that oxygenic and anoxygenic photosynthesis coexisted early on in cyanobacterial evolution. The occurrence of these organisms in Antarctic lakes under euxinic conditions offers a natural laboratory for studying the physiology and adaptation of the first oxygenic photosynthetic organisms.
Research Center/Unit :
InBios - Integrative Biological Sciences - ULiège
Disciplines :
Microbiology
Author, co-author :
Hambücken, Louise ; Université de Liège - ULiège > Integrative Biological Sciences (InBioS)
Sudianto, Edi ; Université de Liège - ULiège > Integrative Biological Sciences (InBioS)
Verleyen, Elie; Protistology and Aquatic Ecology, Ghent University, Ghent, Belgium
Saw, Jimmy H; Department of Biological Sciences, The George Washington University, Washington, DC, USA
Baurain, Denis ; Université de Liège - ULiège > Département des sciences de la vie > Phylogénomique des eucaryotes
Cornet, Luc ; Université de Liège - ULiège > Département des sciences de la vie > Phylogénomique des eucaryotes
Language :
English
Title :
An early diverging SQR enzyme in Antarctic Gloeobacterales indicates sulfide tolerance in thylakoid-lacking cyanobacteria.
Publication date :
13 May 2026
Journal title :
Microbiology Spectrum
eISSN :
2165-0497
Publisher :
American Society for Microbiology, United States
Pages :
e0042326
Peer reviewed :
Peer Reviewed verified by ORBi
Tags :
CÉCI : Consortium des Équipements de Calcul Intensif
PDR T.0018.24 OR-OX-PHOT-IN-CYN; FRIA; Grant no. 2.5020.11
Funding text :
This work was supported by a research grant (PDR T.0018.24 OR-OX-PHOT-IN-CYN) from the Belgian National Fund for Scientific Research (Fonds de la Recherche Scientifique [F.R.S.-FNRS]) to D.B. L.C. is supported by a mandate from the Belgian National Fund for Scientific Research (F.R.S.-FNRS). L.H. is a FRIA grantee of the Fonds de la Recherche Scientifique – F.R.S.-FNRS. Computational resources were provided by the Consortium des Équipements de Calcul Intensif, funded by the F.R.S.-FNRS under grant no. 2.5020.11 and by the Walloon Region.
Supplemental materials and methods and additional phylogenetic trees are provided as supplemental material accompanying this article. All data generated and analyzed in this study have been deposited in Figshare and are accessible via this link: https://doi.org/10.6084/m9.figshare.31333204. The repository includes the complete data set, alignment files, phylogenetic trees (Newick format), and associated analysis files.
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