Manganese and iron deficiency in Southern Ocean Phaeocystis antarctica populations revealed through taxon-specific protein indicators

Miao Wu; J. Scott P. McCain; Elden Rowland; Rob Middag; Mats Sandgren; Andrew E. Allen; Erin M. Bertrand

doi:10.1038/s41467-019-11426-z

Manganese and iron deficiency in Southern Ocean Phaeocystis antarctica populations revealed through taxon-specific protein indicators

Miao Wu, J. Scott P. McCain, Elden Rowland, Rob Middag, Mats Sandgren, Andrew E. Allen, Erin M. Bertrand

Medicine

Producción científica: Contribución a una revista › Artículo › revisión exhaustiva

55 Citas (Scopus)

Resumen

Iron and light are recognized as limiting factors controlling Southern Ocean phytoplankton growth. Recent field-based evidence suggests, however, that manganese availability may also play a role. Here we examine the influence of iron and manganese on protein expression and physiology in Phaeocystis antarctica, a key Antarctic primary producer. We provide taxon-specific proteomic evidence to show that in-situ Southern Ocean Phaeocystis populations regularly experience stress due to combined low manganese and iron availability. In culture, combined low iron and manganese induce large-scale changes in the Phaeocystis proteome and result in reorganization of the photosynthetic apparatus. Natural Phaeocystis populations produce protein signatures indicating late-season manganese and iron stress, consistent with concurrently observed stimulation of chlorophyll production upon additions of manganese or iron. These results implicate manganese as an important driver of Southern Ocean productivity and demonstrate the utility of peptide mass spectrometry for identifying drivers of incomplete macronutrient consumption.

Idioma original	English
Número de artículo	3582
Publicación	Nature Communications
Volumen	10
N.º	1
DOI	https://doi.org/10.1038/s41467-019-11426-z
Estado	Published - dic. 1 2019

Nota bibliográfica

Funding Information:
We thank David Hutchins, Jeff Hoffman, Rachel Sipler, Jenna Spackeen, and Deborah Bronk, as well as Antarctic Support Contractors and the staff at McMurdo Station for support in the field; Jorg Behnke for culturing assistance; Loay Jabre and Julie LaRoche for helpful discussions; and Alejandro Cohen and the Dalhousie Core MS Facility for Orbitrap MS contributions. We are indebted to Sara Bender and Mak Saito for early access to Phaeocystis transcriptome assemblies. J.S.P.M. acknowledges support from the NSERC CREATE Transatlantic Ocean Science and Technology Program. This project was financially supported by NSERC Discovery Grant RGPIN-2015-05009 to E.M.B., Simons Foundation Grant 504183 to E.M.B., an NSERC CGS Postgraduate scholarship to J.S.P.M., Swedish Research Council for sustainable development Formas starting mobility grant 2013-660 to M.W., NSF Polar Programs Fellowship to E.M.B., NSF-ANT-1043671, NSF-OCE-1756884, and Gordon and Betty Moore Foundation Grant GBMF3828 to A.E.A.

Publisher Copyright:
© 2019, The Author(s).

ASJC Scopus Subject Areas

General Chemistry
General Biochemistry,Genetics and Molecular Biology
General Physics and Astronomy

PubMed: MeSH publication types

Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

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10.1038/s41467-019-11426-z

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title = "Manganese and iron deficiency in Southern Ocean Phaeocystis antarctica populations revealed through taxon-specific protein indicators",

abstract = "Iron and light are recognized as limiting factors controlling Southern Ocean phytoplankton growth. Recent field-based evidence suggests, however, that manganese availability may also play a role. Here we examine the influence of iron and manganese on protein expression and physiology in Phaeocystis antarctica, a key Antarctic primary producer. We provide taxon-specific proteomic evidence to show that in-situ Southern Ocean Phaeocystis populations regularly experience stress due to combined low manganese and iron availability. In culture, combined low iron and manganese induce large-scale changes in the Phaeocystis proteome and result in reorganization of the photosynthetic apparatus. Natural Phaeocystis populations produce protein signatures indicating late-season manganese and iron stress, consistent with concurrently observed stimulation of chlorophyll production upon additions of manganese or iron. These results implicate manganese as an important driver of Southern Ocean productivity and demonstrate the utility of peptide mass spectrometry for identifying drivers of incomplete macronutrient consumption.",

author = "Miao Wu and McCain, {J. Scott P.} and Elden Rowland and Rob Middag and Mats Sandgren and Allen, {Andrew E.} and Bertrand, {Erin M.}",

note = "Funding Information: We thank David Hutchins, Jeff Hoffman, Rachel Sipler, Jenna Spackeen, and Deborah Bronk, as well as Antarctic Support Contractors and the staff at McMurdo Station for support in the field; Jorg Behnke for culturing assistance; Loay Jabre and Julie LaRoche for helpful discussions; and Alejandro Cohen and the Dalhousie Core MS Facility for Orbitrap MS contributions. We are indebted to Sara Bender and Mak Saito for early access to Phaeocystis transcriptome assemblies. J.S.P.M. acknowledges support from the NSERC CREATE Transatlantic Ocean Science and Technology Program. This project was financially supported by NSERC Discovery Grant RGPIN-2015-05009 to E.M.B., Simons Foundation Grant 504183 to E.M.B., an NSERC CGS Postgraduate scholarship to J.S.P.M., Swedish Research Council for sustainable development Formas starting mobility grant 2013-660 to M.W., NSF Polar Programs Fellowship to E.M.B., NSF-ANT-1043671, NSF-OCE-1756884, and Gordon and Betty Moore Foundation Grant GBMF3828 to A.E.A. Publisher Copyright: {\textcopyright} 2019, The Author(s).",

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AU - Wu, Miao

AU - McCain, J. Scott P.

AU - Rowland, Elden

AU - Middag, Rob

AU - Sandgren, Mats

AU - Allen, Andrew E.

AU - Bertrand, Erin M.

N1 - Funding Information: We thank David Hutchins, Jeff Hoffman, Rachel Sipler, Jenna Spackeen, and Deborah Bronk, as well as Antarctic Support Contractors and the staff at McMurdo Station for support in the field; Jorg Behnke for culturing assistance; Loay Jabre and Julie LaRoche for helpful discussions; and Alejandro Cohen and the Dalhousie Core MS Facility for Orbitrap MS contributions. We are indebted to Sara Bender and Mak Saito for early access to Phaeocystis transcriptome assemblies. J.S.P.M. acknowledges support from the NSERC CREATE Transatlantic Ocean Science and Technology Program. This project was financially supported by NSERC Discovery Grant RGPIN-2015-05009 to E.M.B., Simons Foundation Grant 504183 to E.M.B., an NSERC CGS Postgraduate scholarship to J.S.P.M., Swedish Research Council for sustainable development Formas starting mobility grant 2013-660 to M.W., NSF Polar Programs Fellowship to E.M.B., NSF-ANT-1043671, NSF-OCE-1756884, and Gordon and Betty Moore Foundation Grant GBMF3828 to A.E.A. Publisher Copyright: © 2019, The Author(s).

PY - 2019/12/1

Y1 - 2019/12/1

N2 - Iron and light are recognized as limiting factors controlling Southern Ocean phytoplankton growth. Recent field-based evidence suggests, however, that manganese availability may also play a role. Here we examine the influence of iron and manganese on protein expression and physiology in Phaeocystis antarctica, a key Antarctic primary producer. We provide taxon-specific proteomic evidence to show that in-situ Southern Ocean Phaeocystis populations regularly experience stress due to combined low manganese and iron availability. In culture, combined low iron and manganese induce large-scale changes in the Phaeocystis proteome and result in reorganization of the photosynthetic apparatus. Natural Phaeocystis populations produce protein signatures indicating late-season manganese and iron stress, consistent with concurrently observed stimulation of chlorophyll production upon additions of manganese or iron. These results implicate manganese as an important driver of Southern Ocean productivity and demonstrate the utility of peptide mass spectrometry for identifying drivers of incomplete macronutrient consumption.

AB - Iron and light are recognized as limiting factors controlling Southern Ocean phytoplankton growth. Recent field-based evidence suggests, however, that manganese availability may also play a role. Here we examine the influence of iron and manganese on protein expression and physiology in Phaeocystis antarctica, a key Antarctic primary producer. We provide taxon-specific proteomic evidence to show that in-situ Southern Ocean Phaeocystis populations regularly experience stress due to combined low manganese and iron availability. In culture, combined low iron and manganese induce large-scale changes in the Phaeocystis proteome and result in reorganization of the photosynthetic apparatus. Natural Phaeocystis populations produce protein signatures indicating late-season manganese and iron stress, consistent with concurrently observed stimulation of chlorophyll production upon additions of manganese or iron. These results implicate manganese as an important driver of Southern Ocean productivity and demonstrate the utility of peptide mass spectrometry for identifying drivers of incomplete macronutrient consumption.

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Manganese and iron deficiency in Southern Ocean Phaeocystis antarctica populations revealed through taxon-specific protein indicators

Resumen

Nota bibliográfica

ASJC Scopus Subject Areas

PubMed: MeSH publication types

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