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Microbial iron and carbon metabolism as revealed by taxonomy-specific functional diversity in the Southern Ocean

Abstract

Marine microbes are major drivers of all elemental cycles. The processing of organic carbon by heterotrophic prokaryotes is tightly coupled to the availability of the trace element iron in large regions of the Southern Ocean. However, the functional diversity in iron and carbon metabolism within diverse communities remains a major unresolved issue. Using novel Southern Ocean meta-omics resources including 133 metagenome-assembled genomes (MAGs), we show a mosaic of taxonomy-specific ecological strategies in naturally iron-fertilized and high nutrient low chlorophyll (HNLC) waters. Taxonomic profiling revealed apparent community shifts across contrasting nutrient regimes. Community-level and genome-resolved metatranscriptomics evidenced a moderate association between taxonomic affiliations and iron and carbon-related functional roles. Diverse ecological strategies emerged when considering the central metabolic pathways of individual MAGs. Closely related lineages appear to adapt to distinct ecological niches, based on their distribution and gene regulation patterns. Our in-depth observations emphasize the complex interplay between the genetic repertoire of individual taxa and their environment and how this shapes prokaryotic responses to iron and organic carbon availability in the Southern Ocean.

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Fig. 1: Genomic features of the 133 Southern Ocean (SO) metagenome-assembled genomes (MAGs) visualized using the circlize package (v0.4.9) in R (v3.6.1).
Fig. 2: Community functional diversity and taxonomic composition within functional groups.
Fig. 3: Statistics of significantly differentially expressed genes (SDEGs) involved in glycoside hydrolysis and key iron metabolic pathways.
Fig. 4: Ratios of ribosomal-protein versus all transcripts (L−1 Mbp−1) from 133 MAGs.
Fig. 5: The distribution of significantly differentially expressed genes (SDEGs) in the MAGs among diverse functional categories related to iron uptake and carbon metabolism.

Data availability

The data sets generated and analysed during the current study are available in the European Nucleotide Archive (ENA) repository at https://www.ebi.ac.uk/ena under the project ID PRJEB37465 (metagenome) and PRJEB37466 (metatranscriptome). The metagenome reads are under the accession number ERR4234198- 4234200. The metatranscriptome reads are under the accession number ERR4234183-4234191. The 949 228 contigs are under the accession number ERZ1694383. The 133 MAGs are under the accession number ERZ1694384-1694516.

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Acknowledgements

We thank B. Quéguiner, the PI of the MOBYDICK project, for providing us the opportunity to participate to this cruise, the captain and crew of the R/V Marion Dufresne for their enthusiasm and support aboard during the MOBYDICK–THEMISTO cruise (https://doi.org/10.17600/18000403). This work was supported by the French oceanographic fleet (“Flotte océanographique française”), the French ANR (“Agence Nationale de la Recherche”, AAPG 2017 program, MOBYDICK Project number: ANR-17-CE01-0013), the French Research program of INSU-CNRS-LEFE/CYBER (“Les enveloppes fluides et l’environnement” - “Cycles biogéochimiques,environnement et ressources”) and the Austrian FWF grant under the number P28781-B21. The authors thank the Roscoff Analyses and Bioinformatics for Marine Sciences Platform (ABiMS; http://abims.sb-roscoff.fr/) and the French Institute of Bioinformatics (IFB; https://www.france-bioinformatique.fr) for providing computational facilities and technical supports. We thank S. Blain for providing the satellite-based chlorophyll a data for the period 1998-2017. We also thank M. A. Moran and M. Landa for providing the internal standards for further in vitro transcription. Two reviewers provided detailed and insightful comments that helped to improve previous versions of our manuscript.

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IO conceived the project and designed the experiments. PD and IO participated to the cruise. PD collected the samples and carried out the nucleic acid extraction. PD performed metagenome read processing and contig assembly. YS carried out bioinformatics analysis. YS and IO wrote the manuscript, and PD provided input to the results and commented on the manuscript.

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Correspondence to Ying Sun.

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Sun, Y., Debeljak, P. & Obernosterer, I. Microbial iron and carbon metabolism as revealed by taxonomy-specific functional diversity in the Southern Ocean. ISME J 15, 2933–2946 (2021). https://doi.org/10.1038/s41396-021-00973-3

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