Coccolithovirus facilitation of carbon export in the North Atlantic

Christien P. Laber; Jonathan E. Hunter; Filipa Carvalho; James R. Collins; Elias J. Hunter; Brittany M. Schieler; Emmanuel Boss; Kuldeep More; Miguel Frada; Kimberlee Thamatrakoln; Christopher M. Brown; Liti Haramaty; Justin Ossolinski; Helen Fredricks; Jozef I. Nissimov; Rebecca Vandzura; Uri Sheyn; Yoav Lehahn; Robert J. Chant; Ana M. Martins; Marco J.L. Coolen; Assaf Vardi; Giacomo R. Ditullio; Benjamin A.S. Van Mooy; Kay D. Bidle

doi:10.1038/s41564-018-0128-4

Coccolithovirus facilitation of carbon export in the North Atlantic

Christien P. Laber, Jonathan E. Hunter, Filipa Carvalho, James R. Collins, Elias J. Hunter, Brittany M. Schieler, Emmanuel Boss, Kuldeep More, Miguel Frada, Kimberlee Thamatrakoln, Christopher M. Brown, Liti Haramaty, Justin Ossolinski, Helen Fredricks, Jozef I. Nissimov, Rebecca Vandzura, Uri Sheyn, Yoav Lehahn, Robert J. Chant, Ana M. MartinsMarco J.L. Coolen, Assaf Vardi, Giacomo R. Ditullio, Benjamin A.S. Van Mooy, Kay D. Bidle^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

80 Scopus citations

Abstract

Marine phytoplankton account for approximately half of global primary productivity ¹ , making their fate an important driver of the marine carbon cycle. Viruses are thought to recycle more than one-quarter of oceanic photosynthetically fixed organic carbon ² , which can stimulate nutrient regeneration, primary production and upper ocean respiration ² via lytic infection and the 'virus shunt'. Ultimately, this limits the trophic transfer of carbon and energy to both higher food webs and the deep ocean ² . Using imagery taken by the Moderate Resolution Imaging Spectroradiometer (MODIS) onboard the Aqua satellite, along with a suite of diagnostic lipid-and gene-based molecular biomarkers, in situ optical sensors and sediment traps, we show that Coccolithovirus infections of mesoscale (~100 km) Emiliania huxleyi blooms in the North Atlantic are coupled with particle aggregation, high zooplankton grazing and greater downward vertical fluxes of both particulate organic and particulate inorganic carbon from the upper mixed layer. Our analyses captured blooms in different phases of infection (early, late and post) and revealed the highest export flux in 'early-infected blooms' with sinking particles being disproportionately enriched with infected cells and subsequently remineralized at depth in the mesopelagic. Our findings reveal viral infection as a previously unrecognized ecosystem process enhancing biological pump efficiency.

Original language	American English
Pages (from-to)	537-547
Number of pages	11
Journal	Nature Microbiology
Volume	3
Issue number	5
DOIs	https://doi.org/10.1038/s41564-018-0128-4
State	Published - 1 May 2018

Bibliographical note

Funding Information:
We thank the captain and crew of the RV Knorr for assistance and cooperation at sea, as well as Marine Facilities and Operations at the Woods Hole Oceanographic Institution for logistical support. We thank R. Fernandes and S. Prakya (University of the Azores) and I. Bashmachnikov (Saint Petersburg University) for daily downloading and sending MODIS and AVISO altimetry data to the RV Knorr for onboard processing. We also thank B. Edwards for logistical help with sediment trap deployments and recoveries. R. Stevens (College of Charleston) and A. Neeley (NASA) provided assistance with the dilution experiments and CHEMTAX analyses, respectively. This study was supported by grants from the National Science Foundation to K.D.B. (OCE-1061876, OCE-1537951 and OCE-1459200), M.J.L.C., G.R.D., A.V. and B.A.S.V.M. (OCE-1050995), and R.J.C. and E.J.H. (OCE-1325258), and from the Gordon and Betty Moore Foundation to K.D.B. (GBMF3789) and B.A.S.V.M. (GBMF3301).

Publisher Copyright:
© 2018 The Author(s).

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10.1038/s41564-018-0128-4

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Laber, C. P., Hunter, J. E., Carvalho, F., Collins, J. R., Hunter, E. J., Schieler, B. M., Boss, E., More, K., Frada, M., Thamatrakoln, K., Brown, C. M., Haramaty, L., Ossolinski, J., Fredricks, H., Nissimov, J. I., Vandzura, R., Sheyn, U., Lehahn, Y., Chant, R. J., ... Bidle, K. D. (2018). Coccolithovirus facilitation of carbon export in the North Atlantic. Nature Microbiology, 3(5), 537-547. https://doi.org/10.1038/s41564-018-0128-4

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title = "Coccolithovirus facilitation of carbon export in the North Atlantic",

abstract = " Marine phytoplankton account for approximately half of global primary productivity 1 , making their fate an important driver of the marine carbon cycle. Viruses are thought to recycle more than one-quarter of oceanic photosynthetically fixed organic carbon 2 , which can stimulate nutrient regeneration, primary production and upper ocean respiration 2 via lytic infection and the 'virus shunt'. Ultimately, this limits the trophic transfer of carbon and energy to both higher food webs and the deep ocean 2 . Using imagery taken by the Moderate Resolution Imaging Spectroradiometer (MODIS) onboard the Aqua satellite, along with a suite of diagnostic lipid-and gene-based molecular biomarkers, in situ optical sensors and sediment traps, we show that Coccolithovirus infections of mesoscale (~100 km) Emiliania huxleyi blooms in the North Atlantic are coupled with particle aggregation, high zooplankton grazing and greater downward vertical fluxes of both particulate organic and particulate inorganic carbon from the upper mixed layer. Our analyses captured blooms in different phases of infection (early, late and post) and revealed the highest export flux in 'early-infected blooms' with sinking particles being disproportionately enriched with infected cells and subsequently remineralized at depth in the mesopelagic. Our findings reveal viral infection as a previously unrecognized ecosystem process enhancing biological pump efficiency.",

author = "Laber, {Christien P.} and Hunter, {Jonathan E.} and Filipa Carvalho and Collins, {James R.} and Hunter, {Elias J.} and Schieler, {Brittany M.} and Emmanuel Boss and Kuldeep More and Miguel Frada and Kimberlee Thamatrakoln and Brown, {Christopher M.} and Liti Haramaty and Justin Ossolinski and Helen Fredricks and Nissimov, {Jozef I.} and Rebecca Vandzura and Uri Sheyn and Yoav Lehahn and Chant, {Robert J.} and Martins, {Ana M.} and Coolen, {Marco J.L.} and Assaf Vardi and Ditullio, {Giacomo R.} and {Van Mooy}, {Benjamin A.S.} and Bidle, {Kay D.}",

note = "Funding Information: We thank the captain and crew of the RV Knorr for assistance and cooperation at sea, as well as Marine Facilities and Operations at the Woods Hole Oceanographic Institution for logistical support. We thank R. Fernandes and S. Prakya (University of the Azores) and I. Bashmachnikov (Saint Petersburg University) for daily downloading and sending MODIS and AVISO altimetry data to the RV Knorr for onboard processing. We also thank B. Edwards for logistical help with sediment trap deployments and recoveries. R. Stevens (College of Charleston) and A. Neeley (NASA) provided assistance with the dilution experiments and CHEMTAX analyses, respectively. This study was supported by grants from the National Science Foundation to K.D.B. (OCE-1061876, OCE-1537951 and OCE-1459200), M.J.L.C., G.R.D., A.V. and B.A.S.V.M. (OCE-1050995), and R.J.C. and E.J.H. (OCE-1325258), and from the Gordon and Betty Moore Foundation to K.D.B. (GBMF3789) and B.A.S.V.M. (GBMF3301). Publisher Copyright: {\textcopyright} 2018 The Author(s).",

year = "2018",

month = may,

day = "1",

doi = "10.1038/s41564-018-0128-4",

language = "American English",

volume = "3",

pages = "537--547",

journal = "Nature Microbiology",

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Laber, CP, Hunter, JE, Carvalho, F, Collins, JR, Hunter, EJ, Schieler, BM, Boss, E, More, K, Frada, M, Thamatrakoln, K, Brown, CM, Haramaty, L, Ossolinski, J, Fredricks, H, Nissimov, JI, Vandzura, R, Sheyn, U, Lehahn, Y, Chant, RJ, Martins, AM, Coolen, MJL, Vardi, A, Ditullio, GR, Van Mooy, BAS & Bidle, KD 2018, 'Coccolithovirus facilitation of carbon export in the North Atlantic', Nature Microbiology, vol. 3, no. 5, pp. 537-547. https://doi.org/10.1038/s41564-018-0128-4

TY - JOUR

T1 - Coccolithovirus facilitation of carbon export in the North Atlantic

AU - Laber, Christien P.

AU - Hunter, Jonathan E.

AU - Carvalho, Filipa

AU - Collins, James R.

AU - Hunter, Elias J.

AU - Schieler, Brittany M.

AU - Boss, Emmanuel

AU - More, Kuldeep

AU - Frada, Miguel

AU - Thamatrakoln, Kimberlee

AU - Brown, Christopher M.

AU - Haramaty, Liti

AU - Ossolinski, Justin

AU - Fredricks, Helen

AU - Nissimov, Jozef I.

AU - Vandzura, Rebecca

AU - Sheyn, Uri

AU - Lehahn, Yoav

AU - Chant, Robert J.

AU - Martins, Ana M.

AU - Coolen, Marco J.L.

AU - Vardi, Assaf

AU - Ditullio, Giacomo R.

AU - Van Mooy, Benjamin A.S.

AU - Bidle, Kay D.

N1 - Funding Information: We thank the captain and crew of the RV Knorr for assistance and cooperation at sea, as well as Marine Facilities and Operations at the Woods Hole Oceanographic Institution for logistical support. We thank R. Fernandes and S. Prakya (University of the Azores) and I. Bashmachnikov (Saint Petersburg University) for daily downloading and sending MODIS and AVISO altimetry data to the RV Knorr for onboard processing. We also thank B. Edwards for logistical help with sediment trap deployments and recoveries. R. Stevens (College of Charleston) and A. Neeley (NASA) provided assistance with the dilution experiments and CHEMTAX analyses, respectively. This study was supported by grants from the National Science Foundation to K.D.B. (OCE-1061876, OCE-1537951 and OCE-1459200), M.J.L.C., G.R.D., A.V. and B.A.S.V.M. (OCE-1050995), and R.J.C. and E.J.H. (OCE-1325258), and from the Gordon and Betty Moore Foundation to K.D.B. (GBMF3789) and B.A.S.V.M. (GBMF3301). Publisher Copyright: © 2018 The Author(s).

PY - 2018/5/1

Y1 - 2018/5/1

N2 - Marine phytoplankton account for approximately half of global primary productivity 1 , making their fate an important driver of the marine carbon cycle. Viruses are thought to recycle more than one-quarter of oceanic photosynthetically fixed organic carbon 2 , which can stimulate nutrient regeneration, primary production and upper ocean respiration 2 via lytic infection and the 'virus shunt'. Ultimately, this limits the trophic transfer of carbon and energy to both higher food webs and the deep ocean 2 . Using imagery taken by the Moderate Resolution Imaging Spectroradiometer (MODIS) onboard the Aqua satellite, along with a suite of diagnostic lipid-and gene-based molecular biomarkers, in situ optical sensors and sediment traps, we show that Coccolithovirus infections of mesoscale (~100 km) Emiliania huxleyi blooms in the North Atlantic are coupled with particle aggregation, high zooplankton grazing and greater downward vertical fluxes of both particulate organic and particulate inorganic carbon from the upper mixed layer. Our analyses captured blooms in different phases of infection (early, late and post) and revealed the highest export flux in 'early-infected blooms' with sinking particles being disproportionately enriched with infected cells and subsequently remineralized at depth in the mesopelagic. Our findings reveal viral infection as a previously unrecognized ecosystem process enhancing biological pump efficiency.

AB - Marine phytoplankton account for approximately half of global primary productivity 1 , making their fate an important driver of the marine carbon cycle. Viruses are thought to recycle more than one-quarter of oceanic photosynthetically fixed organic carbon 2 , which can stimulate nutrient regeneration, primary production and upper ocean respiration 2 via lytic infection and the 'virus shunt'. Ultimately, this limits the trophic transfer of carbon and energy to both higher food webs and the deep ocean 2 . Using imagery taken by the Moderate Resolution Imaging Spectroradiometer (MODIS) onboard the Aqua satellite, along with a suite of diagnostic lipid-and gene-based molecular biomarkers, in situ optical sensors and sediment traps, we show that Coccolithovirus infections of mesoscale (~100 km) Emiliania huxleyi blooms in the North Atlantic are coupled with particle aggregation, high zooplankton grazing and greater downward vertical fluxes of both particulate organic and particulate inorganic carbon from the upper mixed layer. Our analyses captured blooms in different phases of infection (early, late and post) and revealed the highest export flux in 'early-infected blooms' with sinking particles being disproportionately enriched with infected cells and subsequently remineralized at depth in the mesopelagic. Our findings reveal viral infection as a previously unrecognized ecosystem process enhancing biological pump efficiency.

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SP - 537

EP - 547

JO - Nature Microbiology

JF - Nature Microbiology

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ER -

Coccolithovirus facilitation of carbon export in the North Atlantic

Abstract

Bibliographical note

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