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Transcriptional responses of Trichodesmium to natural inverse gradients of Fe and P availability

Transcriptional responses of Trichodesmium to natural inverse gradients of Fe and P availability
Transcriptional responses of Trichodesmium to natural inverse gradients of Fe and P availability
The filamentous diazotrophic cyanobacterium Trichodesmium is responsible for a significant fraction of marine di-nitrogen (N2) fixation. Growth and distribution of Trichodesmium and other diazotrophs in the vast oligotrophic subtropical gyres is influenced by iron (Fe) and phosphorus (P) availability, while reciprocally influencing the biogeochemistry of these nutrients. Here we use observations across natural inverse gradients in Fe and P in the North Atlantic subtropical gyre (NASG) to demonstrate how Trichodesmium acclimates in situ to resource availability. Transcriptomic analysis identified progressive upregulation of known iron-stress biomarker genes with decreasing Fe availability, and progressive upregulation of genes involved in the acquisition of diverse P sources with decreasing P availability, while genes involved in N2 fixation were upregulated at the intersection under moderate Fe and P availability. Enhanced N2 fixation within the Fe and P co-stressed transition region was also associated with a distinct, consistent metabolic profile, including the expression of alternative photosynthetic pathways that potentially facilitate ATP generation required for N2 fixation with reduced net oxygen production. The observed response of Trichodesmium to availability of both Fe and P supports suggestions that these biogeochemically significant organisms employ unique molecular, and thus physiological responses as adaptations to specifically exploit the Fe and P co-limited niche they construct.
1751-7362
1-10
Cerdan Garcia, Elena
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Baylay, Alison
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Polyviou, Despo
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Woodward, E.M.S.
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Wrightson, Lewis
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Mahaffey, Claire
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Lohan, Maeve
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Moore, Christopher
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Bibby, Thomas
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Robidart, Julie C.
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Cerdan Garcia, Elena
7171170a-2128-4369-87c3-cffddea2e414
Baylay, Alison
08ea69f8-9910-4c8b-86a9-602e45b8a44e
Polyviou, Despo
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Woodward, E.M.S.
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Wrightson, Lewis
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Mahaffey, Claire
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Lohan, Maeve
6ca10597-2d0f-40e8-8e4f-7619dfac5088
Moore, Christopher
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Bibby, Thomas
e04ea079-dd90-4ead-9840-00882de27ebd
Robidart, Julie C.
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Cerdan Garcia, Elena, Baylay, Alison, Polyviou, Despo, Woodward, E.M.S., Wrightson, Lewis, Mahaffey, Claire, Lohan, Maeve, Moore, Christopher, Bibby, Thomas and Robidart, Julie C. (2021) Transcriptional responses of Trichodesmium to natural inverse gradients of Fe and P availability. The ISME Journal, 1-10. (doi:10.1038/s41396-021-01151-1).

Record type: Article

Abstract

The filamentous diazotrophic cyanobacterium Trichodesmium is responsible for a significant fraction of marine di-nitrogen (N2) fixation. Growth and distribution of Trichodesmium and other diazotrophs in the vast oligotrophic subtropical gyres is influenced by iron (Fe) and phosphorus (P) availability, while reciprocally influencing the biogeochemistry of these nutrients. Here we use observations across natural inverse gradients in Fe and P in the North Atlantic subtropical gyre (NASG) to demonstrate how Trichodesmium acclimates in situ to resource availability. Transcriptomic analysis identified progressive upregulation of known iron-stress biomarker genes with decreasing Fe availability, and progressive upregulation of genes involved in the acquisition of diverse P sources with decreasing P availability, while genes involved in N2 fixation were upregulated at the intersection under moderate Fe and P availability. Enhanced N2 fixation within the Fe and P co-stressed transition region was also associated with a distinct, consistent metabolic profile, including the expression of alternative photosynthetic pathways that potentially facilitate ATP generation required for N2 fixation with reduced net oxygen production. The observed response of Trichodesmium to availability of both Fe and P supports suggestions that these biogeochemically significant organisms employ unique molecular, and thus physiological responses as adaptations to specifically exploit the Fe and P co-limited niche they construct.

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Submitted date: 15 April 2021
Accepted/In Press date: 1 November 2021
e-pub ahead of print date: 24 November 2021
Published date: 24 November 2021
Additional Information: Funding Information: We would like to thank the Captain and crew of the RRS James Cook JC150, as well as K. Kunde, N. Wyatt, J. Harley, N. Held and S. Sargent for sampling and nutrient analysis assistance. This work was supported by the UK NERC funded project “Zinc Iron and Phosphorus Co-Limitation in the Ocean (ZIPLOc) (NE/N001079/1) to CM and ML that provided nutrient analysis, N2 fixation rates and ancillary oceanographic data. Supporting funding for molecular sampling and analysis came from UK NERC grant MARINeDNA (NE/N006151/1) and EU-H2020 Project AtlantOS (Grant Agreement No. 633211) (JCR). ECG is the recipient of a Graduate School of the National Oceanography Centre Southampton PhD studentship. Publisher Copyright: © 2021, The Author(s).

Identifiers

Local EPrints ID: 455141
URI: http://eprints.soton.ac.uk/id/eprint/455141
ISSN: 1751-7362
PURE UUID: 061653ca-c6ee-47b2-a6d3-d7dd21378f86
ORCID for Elena Cerdan Garcia: ORCID iD orcid.org/0000-0002-0409-7722
ORCID for Alison Baylay: ORCID iD orcid.org/0000-0002-0814-0740
ORCID for Maeve Lohan: ORCID iD orcid.org/0000-0002-5340-3108
ORCID for Christopher Moore: ORCID iD orcid.org/0000-0002-9541-6046

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Date deposited: 10 Mar 2022 18:27
Last modified: 17 Mar 2024 03:31

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Contributors

Author: Alison Baylay ORCID iD
Author: Despo Polyviou
Author: E.M.S. Woodward
Author: Lewis Wrightson
Author: Claire Mahaffey
Author: Maeve Lohan ORCID iD
Author: Thomas Bibby
Author: Julie C. Robidart

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