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Molecular mechanisms underlying iron and phosphorus co-limitation responses in the nitrogen-fixing cyanobacterium Crocosphaera

Abstract

In the nitrogen-limited subtropical gyres, diazotrophic cyanobacteria, including Crocosphaera, provide an essential ecosystem service by converting dinitrogen (N2) gas into ammonia to support primary production in these oligotrophic regimes. Natural gradients of phosphorus (P) and iron (Fe) availability in the low-latitude oceans constrain the biogeography and activity of diazotrophs with important implications for marine biogeochemical cycling. Much remains unknown regarding Crocosphaera’s physiological and molecular responses to multiple nutrient limitations. We cultured C. watsonii under Fe, P, and Fe/P (co)-limiting scenarios to link cellular physiology with diel gene expression and observed unique physiological and transcriptional profiles for each treatment. Counterintuitively, reduced growth and N2 fixation resource use efficiencies (RUEs) for Fe or P under P limitation were alleviated under Fe/P co-limitation. Differential gene expression analyses show that Fe/P co-limited cells employ the same responses as single-nutrient limited cells that reduce cellular nutrient requirements and increase responsiveness to environmental change including smaller cell size, protein turnover (Fe-limited), and upregulation of environmental sense-and-respond systems (P-limited). Combined, these mechanisms enhance growth and RUEs in Fe/P co-limited cells. These findings are important to our understanding of nutrient controls on N2 fixation and the implications for primary productivity and microbial dynamics in a changing ocean.

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Fig. 1: Nutrient replete and nutrient-limited Crocosphaera physiology.
Fig. 2: Calculated elemental use efficiencies (RUEs, mol C or N fixed/hour/mol intracellular P or Fe) of nutrient replete and nutrient-limited Crocosphaera.
Fig. 3: Gene expression trends of commonly used Fe- and P limitation biomarkers.
Fig. 4: Diel transcriptomes and core functional enrichment analysis of differentially expressed genes.
Fig. 5: A schematic of the different strategies and mechanisms to manage single-nutrient limitation (Fe-limited or P-limited) and Fe/P co-limited conditions.

Data availability

The physiological data collected from this study are available from BCO-DMO online (http://bcodmo.org). Raw RNAseq reads for differential gene expression analyses are deposited at NCBI’s SRA under BioProject PRJNA807802. All scripts to recreate the differential gene expression analyses, statistical analyses, and visualizations are available at https://github.com/yang-nina/CrocosphaeraFePColimitation.

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Acknowledgements

This research was supported by U.S. National Science Foundation Biological Oceanography program grants OCE 1657757, OCE 1851222 to DAH, FXF, and EAW, OCE 2149837 to DAH and FXF, SCOR Working Group 149, as well as graduate student support from a USC Provost Fellowship to NY. We would also like to thank three anonymous reviewers who provided comments to improve this manuscript.

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NY, F-FX, P-PQ, and DAH designed the experiment. NY carried out the experiment, with significant support from Y-AL, CAM, and MAD in monitoring cultures using cell-based growth rates and experimental maintenance. P-PQ and F-XF also contributed to experimental maintenance and support with physiological data analysis. NY collected large-volume samples, extracted RNA for transcriptomics analyses, and conducted differential gene expression analyses with support from P-PQ and EAW. NY wrote the manuscript with input from EAW and DAH. All authors reviewed and gave their approval for the final manuscript.

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Correspondence to David A. Hutchins.

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Yang, N., Lin, YA., Merkel, C.A. et al. Molecular mechanisms underlying iron and phosphorus co-limitation responses in the nitrogen-fixing cyanobacterium Crocosphaera. ISME J 16, 2702–2711 (2022). https://doi.org/10.1038/s41396-022-01307-7

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