Elevated temperature increases carbon and nitrogen fluxes between phytoplankton and heterotrophic bacteria through physical attachment

Nestor Arandia-Gorostidi; Peter K Weber; Laura Alonso-Sáez; Xose Anxelu G. Moran; Xavier Mayali

doi:10.1038/ismej.2016.156

Elevated temperature increases carbon and nitrogen fluxes between phytoplankton and heterotrophic bacteria through physical attachment

Nestor Arandia-Gorostidi, Peter K Weber, Laura Alonso-Sáez, Xose Anxelu G. Moran, Xavier Mayali

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67 Scopus citations

Abstract

Quantifying the contribution of marine microorganisms to carbon and nitrogen cycles and their response to predicted ocean warming is one of the main challenges of microbial oceanography. Here we present a single-cell NanoSIMS isotope analysis to quantify C and N uptake by free-living and attached phytoplankton and heterotrophic bacteria, and their response to short-term experimental warming of 4 °C. Elevated temperature increased total C fixation by over 50%, a small but significant fraction of which was transferred to heterotrophs within 12 h. Cell-to-cell attachment doubled the secondary C uptake by heterotrophic bacteria and increased secondary N incorporation by autotrophs by 68%. Warming also increased the abundance of phytoplankton with attached heterotrophs by 80%, and promoted C transfer from phytoplankton to bacteria by 17% and N transfer from bacteria to phytoplankton by 50%. Our results indicate that phytoplankton-bacteria attachment provides an ecological advantage for nutrient incorporation, suggesting a mutualistic relationship that appears to be enhanced by temperature increases.

Original language	English (US)
Pages (from-to)	641-650
Number of pages	10
Journal	The ISME Journal
Volume	11
Issue number	3
DOIs	https://doi.org/10.1038/ismej.2016.156
State	Published - Dec 6 2016

Bibliographical note

KAUST Repository Item: Exported on 2020-10-01
Acknowledgements: This work was partially supported by COMITE project by Spanish National Investigation+Development+Innovation (I+D+I). Financial support for NAG’s PhD fellowship was provided by the Basque Government. LAS was supported by a ‘Juan de la Cierva’ fellowship from the Spanish Ministry of Science and Education and a Marie Curie Reintegration Grant (FP7, Grant Agreement 268331). XM was partially supported by the Gordon and Betty Moore Foundation Marine Microbiology Initiative grant #3302, and method development at LLNL was funded by the Department of Energy’s Genome Sciences Program grant SCW1039. Work at LLNL was performed under the auspices of the US Department of Energy at Lawrence Livermore National Laboratory under Contract DE-AC52-07NA27344.

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10.1038/ismej.2016.156

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title = "Elevated temperature increases carbon and nitrogen fluxes between phytoplankton and heterotrophic bacteria through physical attachment",

abstract = "Quantifying the contribution of marine microorganisms to carbon and nitrogen cycles and their response to predicted ocean warming is one of the main challenges of microbial oceanography. Here we present a single-cell NanoSIMS isotope analysis to quantify C and N uptake by free-living and attached phytoplankton and heterotrophic bacteria, and their response to short-term experimental warming of 4 °C. Elevated temperature increased total C fixation by over 50%, a small but significant fraction of which was transferred to heterotrophs within 12 h. Cell-to-cell attachment doubled the secondary C uptake by heterotrophic bacteria and increased secondary N incorporation by autotrophs by 68%. Warming also increased the abundance of phytoplankton with attached heterotrophs by 80%, and promoted C transfer from phytoplankton to bacteria by 17% and N transfer from bacteria to phytoplankton by 50%. Our results indicate that phytoplankton-bacteria attachment provides an ecological advantage for nutrient incorporation, suggesting a mutualistic relationship that appears to be enhanced by temperature increases.",

author = "Nestor Arandia-Gorostidi and Weber, {Peter K} and Laura Alonso-S{\'a}ez and Moran, {Xose Anxelu G.} and Xavier Mayali",

note = "KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: This work was partially supported by COMITE project by Spanish National Investigation+Development+Innovation (I+D+I). Financial support for NAG{\textquoteright}s PhD fellowship was provided by the Basque Government. LAS was supported by a {\textquoteleft}Juan de la Cierva{\textquoteright} fellowship from the Spanish Ministry of Science and Education and a Marie Curie Reintegration Grant (FP7, Grant Agreement 268331). XM was partially supported by the Gordon and Betty Moore Foundation Marine Microbiology Initiative grant #3302, and method development at LLNL was funded by the Department of Energy{\textquoteright}s Genome Sciences Program grant SCW1039. Work at LLNL was performed under the auspices of the US Department of Energy at Lawrence Livermore National Laboratory under Contract DE-AC52-07NA27344.",

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AU - Arandia-Gorostidi, Nestor

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AU - Alonso-Sáez, Laura

AU - Moran, Xose Anxelu G.

AU - Mayali, Xavier

N1 - KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: This work was partially supported by COMITE project by Spanish National Investigation+Development+Innovation (I+D+I). Financial support for NAG’s PhD fellowship was provided by the Basque Government. LAS was supported by a ‘Juan de la Cierva’ fellowship from the Spanish Ministry of Science and Education and a Marie Curie Reintegration Grant (FP7, Grant Agreement 268331). XM was partially supported by the Gordon and Betty Moore Foundation Marine Microbiology Initiative grant #3302, and method development at LLNL was funded by the Department of Energy’s Genome Sciences Program grant SCW1039. Work at LLNL was performed under the auspices of the US Department of Energy at Lawrence Livermore National Laboratory under Contract DE-AC52-07NA27344.

PY - 2016/12/6

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N2 - Quantifying the contribution of marine microorganisms to carbon and nitrogen cycles and their response to predicted ocean warming is one of the main challenges of microbial oceanography. Here we present a single-cell NanoSIMS isotope analysis to quantify C and N uptake by free-living and attached phytoplankton and heterotrophic bacteria, and their response to short-term experimental warming of 4 °C. Elevated temperature increased total C fixation by over 50%, a small but significant fraction of which was transferred to heterotrophs within 12 h. Cell-to-cell attachment doubled the secondary C uptake by heterotrophic bacteria and increased secondary N incorporation by autotrophs by 68%. Warming also increased the abundance of phytoplankton with attached heterotrophs by 80%, and promoted C transfer from phytoplankton to bacteria by 17% and N transfer from bacteria to phytoplankton by 50%. Our results indicate that phytoplankton-bacteria attachment provides an ecological advantage for nutrient incorporation, suggesting a mutualistic relationship that appears to be enhanced by temperature increases.

AB - Quantifying the contribution of marine microorganisms to carbon and nitrogen cycles and their response to predicted ocean warming is one of the main challenges of microbial oceanography. Here we present a single-cell NanoSIMS isotope analysis to quantify C and N uptake by free-living and attached phytoplankton and heterotrophic bacteria, and their response to short-term experimental warming of 4 °C. Elevated temperature increased total C fixation by over 50%, a small but significant fraction of which was transferred to heterotrophs within 12 h. Cell-to-cell attachment doubled the secondary C uptake by heterotrophic bacteria and increased secondary N incorporation by autotrophs by 68%. Warming also increased the abundance of phytoplankton with attached heterotrophs by 80%, and promoted C transfer from phytoplankton to bacteria by 17% and N transfer from bacteria to phytoplankton by 50%. Our results indicate that phytoplankton-bacteria attachment provides an ecological advantage for nutrient incorporation, suggesting a mutualistic relationship that appears to be enhanced by temperature increases.

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Elevated temperature increases carbon and nitrogen fluxes between phytoplankton and heterotrophic bacteria through physical attachment

Abstract

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