Differential global distribution of marine picocyanobacteria gene clusters reveals distinct niche-related adaptive strategies

Hugo Doré , Ulysse Guyet (1) , Jade Leconte (2) , Gregory Farrant (1) , Benjamin Alric (3) , Morgane Ratin (1, 4) , Martin Ostrowski , Mathilde Ferrieux (1) , Loraine Brillet-Guéguen (5, 4, 6) , Mark Hoebeke , Jukka Siltanen (7, 6, 4) , Gildas Le Corguillé (4) , Erwan Corre (6, 7, 4) , Patrick Wincker (8, 9) , David Scanlan (10) , Damien Eveillard (11, 12) , Frédéric Partensky (1, 4) , Laurence Garczarek (1, 4)

1 ADMM - Adaptation et diversité en milieu marin
2 UMR 8030 - Génomique métabolique
3 CARRTEL - Centre Alpin de Recherche sur les Réseaux Trophiques et Ecosystèmes Limniques
4 SBR - Station biologique de Roscoff = Roscoff Marine Station
5 LBI2M - Laboratoire de Biologie Intégrative des Modèles Marins
6 FR2424 - Fédération de recherche de Roscoff
7 ABIMS - ABiMS - Informatique et bioinformatique = Analysis and Bioinformatics for Marine Science
8 GENOSCOPE - Genoscope - Centre national de séquençage [Evry]
9 GOSEE - Global Oceans Systems Ecology & Evolution - Tara Oceans
10 University of Warwick [Coventry]
11 LS2N - Laboratoire des Sciences du Numérique de Nantes
12 LS2N - équipe COMBI - Combinatoire et Bioinformatique

Abstract The ever-increasing number of available microbial genomes and metagenomes provides new opportunities to investigate the links between niche partitioning and genome evolution in the ocean, especially for the abundant and ubiquitous marine picocyanobacteria Prochlorococcus and Synechococcus . Here, by combining metagenome analyses of the Tara Oceans dataset with comparative genomics, including phyletic patterns and genomic context of individual genes from 256 reference genomes, we show that picocyanobacterial communities thriving in different niches possess distinct gene repertoires. We also identify clusters of adjacent genes that display specific distribution patterns in the field (eCAGs) and are thus potentially involved in the same metabolic pathway and may have a key role in niche adaptation. Several eCAGs are likely involved in the uptake or incorporation of complex organic forms of nutrients, such as guanidine, cyanate, cyanide, pyrimidine, or phosphonates, which might be either directly used by cells, for example for the biosynthesis of proteins or DNA, or degraded to inorganic nitrogen and/or phosphorus forms. We also highlight the enrichment of eCAGs involved in polysaccharide capsule biosynthesis in Synechococcus populations thriving in both nitrogen- and phosphorus-depleted areas vs. low-iron (Fe) regions, suggesting that the complexes they encode may be too energy-consuming for picocyanobacteria thriving in the latter areas. In contrast, Prochlorococcus populations thriving in Fe-depleted areas specifically possess an alternative respiratory terminal oxidase, potentially involved in the reduction of Fe(III) to Fe(II). Altogether, this study provides insights into how phytoplankton communities populate oceanic ecosystems, which is relevant to understanding their capacity to respond to ongoing climate change.

Mots clés: Prochlorococcus; Synechococcus; niche partitioning; Tara Oceans; metagenomics; Prochlorococcus Synechococcus niche partitioning Tara Oceans metagenomics

Domaines: Biodiversité et Ecologie; Microbiologie et Parasitologie; Bactériologie

Hugo Doré, Ulysse Guyet, Jade Leconte, Gregory Farrant, Benjamin Alric, et al.. Differential global distribution of marine picocyanobacteria gene clusters reveals distinct niche-related adaptive strategies. The International Society of Microbiologial Ecology Journal, 2023, 17 (5), pp.720-732. ⟨10.1038/s41396-023-01386-0⟩. ⟨hal-04238382⟩