Adsorptive exchange of coccolith biominerals facilitates viral infection

Johns, Christopher T.; Bondoc-Naumovitz, Karen Grace; Matthews, Alexandra; Matson, Paul G.; Iglesias-Rodriguez, M. Debora; Taylor, Alison R.; Fuchs, Heidi L.; Bidle, Kay D.

doi:10.1126/sciadv.adc8728

Adsorptive exchange of coccolith biominerals facilitates viral infection

Journal Article · Thu Jan 19 23:00:00 EST 2023 · Science Advances

DOI:https://doi.org/10.1126/sciadv.adc8728· OSTI ID:1997725

^[1]; ^[1]; ^[1]; ^[2]; Iglesias-Rodriguez, M. Debora ^[2]; ^[3]; ^[1]; ^[1]

Rutgers University, New Brunswick, NJ (United States)
University of California, Santa Barbara, CA (United States)
University of North Carolina, Wilmington, NC (United States)

Marine coccolithophores are globally distributed, unicellular phytoplankton that produce nanopatterned, calcite biominerals (coccoliths). These biominerals are synthesized internally, deposited into an extracellular coccosphere, and routinely released into the external medium, where they profoundly affect the global carbon cycle. The cellular costs and benefits of calcification remain unresolved. Here, we show observational and experimental evidence, supported by biophysical modeling, that free coccoliths are highly adsorptive biominerals that readily interact with cells to form chimeric coccospheres and with viruses to form “viroliths,” which facilitate infection. Adsorption to cells is mediated by organic matter associated with the coccolith base plate and varies with biomineral morphology. Biomineral hitchhiking increases host-virus encounters by nearly an order of magnitude and can be the dominant mode of infection under stormy conditions, fundamentally altering how we view biomineral-cell-virus interactions in the environment.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE; Gordon and Betty Moore Foundation; National Science Foundation (NSF); National Aeronautics and Space Administration (NASA); Bureau of Ocean Energy Management (BOEM); National Institutes of Health (NIH)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1997725

Journal Information:: Science Advances, Journal Name: Science Advances Journal Issue: 3 Vol. 9; ISSN 2375-2548

Publisher:: AAASCopyright Statement

Country of Publication:: United States

Language:: English

References (63)

The multiple fates of sinking particles in the North Atlantic Ocean Collins, James R.; Edwards, Bethanie R.; Thamatrakoln, Kimberlee Global Biogeochemical Cycles, Vol. 29, Issue 9 https://doi.org/10.1002/2014GB005037	journal	September 2015
Biogenic calcite particles from microalgae-Coccoliths as a potential raw material Jakob, Ioanna; Chairopoulou, Makrina Artemis; Vučak, Marijan Engineering in Life Sciences, Vol. 17, Issue 6 https://doi.org/10.1002/elsc.201600183	journal	February 2017
Coccolith Ultrastructure and Biomineralisation Young, Jeremy R.; Davis, Sean A.; Bown, Paul R. Journal of Structural Biology, Vol. 126, Issue 3 https://doi.org/10.1006/jsbi.1999.4132	journal	June 1999
Culture of Phytoplankton for Feeding Marine Invertebrates Guillard, Robert R. L. Culture of Marine Invertebrate Animals https://doi.org/10.1007/978-1-4615-8714-9_3	book	January 1975
ggplot2 Wickham, Hadley Use R! https://doi.org/10.1007/978-3-319-24277-4	book	January 2016
Ultrastructural polysaccharide localization in calcifying and naked cells of the coccolithophoridEmiliania huxleyi van der Wal, P.; de Jong, E. W.; Westbroek, P. Protoplasma, Vol. 118, Issue 2 https://doi.org/10.1007/BF01293073	journal	June 1983
Development of a rapid isolation procedure for coccolith ultrafine particles produced by coccolithophorid algae Takano, Hiroyuki; Manabe, Eichi; Hirano, Morio Applied Biochemistry and Biotechnology, Vol. 39-40, Issue 1 https://doi.org/10.1007/BF02918993	journal	September 1993
Size spectra and aggregation of suspended particles in the deep ocean McCave, I. N. Deep Sea Research Part A. Oceanographic Research Papers, Vol. 31, Issue 4 https://doi.org/10.1016/0198-0149(84)90088-8	journal	April 1984
Distribution of living coccolithophore assemblages in the Gulf of Elat ('Aqaba) Winter, Amos; Reiss, Zeev; Luz, Boaz Marine Micropaleontology, Vol. 4 https://doi.org/10.1016/0377-8398(79)90017-3	journal	January 1979
Genotypic variation in the coccolithophorid speciesEmiliania huxleyi Young, Jeremy R.; Westbroek, Peter Marine Micropaleontology, Vol. 18, Issue 1-2 https://doi.org/10.1016/0377-8398(91)90004-P	journal	November 1991
New examples of holococcolith–heterococcolith combination coccospheres and their implications for coccolithophorid biology Cros, L.; Kleijne, A.; Zeltner, A. Marine Micropaleontology, Vol. 39, Issue 1-4 https://doi.org/10.1016/S0377-8398(00)00010-4	journal	June 2000
The effects of light, macronutrients, trace metals and CO2 on the production of calcium carbonate and organic carbon in coccolithophores—A review Zondervan, Ingrid Deep Sea Research Part II: Topical Studies in Oceanography, Vol. 54, Issue 5-7 https://doi.org/10.1016/j.dsr2.2006.12.004	journal	March 2007
An assessment of the mechanisms for the transfer of lead and mercury from atmospherically contaminated organic soils to lake sediments with particular reference to Scotland, UK Rose, Neil L.; Yang, Handong; Turner, Simon D. Geochimica et Cosmochimica Acta, Vol. 82 https://doi.org/10.1016/j.gca.2010.12.026	journal	April 2012
Response of the coccolithophores Emiliania huxleyi and Coccolithus braarudii to changing seawater Mg2+ and Ca2+ concentrations: Mg/Ca, Sr/Ca ratios and δ44/40Ca, δ26/24Mg of coccolith calcite Müller, Marius N.; Kısakürek, Başak; Buhl, Dieter Geochimica et Cosmochimica Acta, Vol. 75, Issue 8 https://doi.org/10.1016/j.gca.2011.01.035	journal	April 2011
Removal of organic magnesium in coccolithophore calcite Blanco-Ameijeiras, S.; Lebrato, M.; Stoll, H. M. Geochimica et Cosmochimica Acta, Vol. 89 https://doi.org/10.1016/j.gca.2012.04.043	journal	July 2012
Dynamics of transparent exopolymeric particles (TEP) production by Phaeocystis globosa under N- or P-limitation: a controlling factor of the retention/export balance Mari, Xavier; Rassoulzadegan, Fereidoun; Brussaard, Corina P. D. Harmful Algae, Vol. 4, Issue 5 https://doi.org/10.1016/j.hal.2004.12.014	journal	August 2005
Seascape-level variation in turbulence- and wave-generated hydrodynamic signals experienced by plankton Fuchs, Heidi L.; Gerbi, Gregory P. Progress in Oceanography, Vol. 141 https://doi.org/10.1016/j.pocean.2015.12.010	journal	February 2016
Coccolithophore biomineralization: New questions, new answers Brownlee, Colin; Wheeler, Glen L.; Taylor, Alison R. Seminars in Cell & Developmental Biology, Vol. 46 https://doi.org/10.1016/j.semcdb.2015.10.027	journal	October 2015
Formation, Development, and Propagation of a Rare Coastal Coccolithophore Bloom Matson, Paul G.; Washburn, Libe; Fields, Erik A. Journal of Geophysical Research: Oceans, Vol. 124, Issue 5 https://doi.org/10.1029/2019JC015072	journal	May 2019
Nitric oxide production and antioxidant function during viral infection of the coccolithophore Emiliania huxleyi Schieler, Brittany M.; Soni, Megha V.; Brown, Christopher M. The ISME Journal, Vol. 13, Issue 4 https://doi.org/10.1038/s41396-018-0325-4	journal	January 2019
Temperate infection in a virus–host system previously known for virulent dynamics Knowles, Ben; Bonachela, Juan A.; Behrenfeld, Michael J. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-18078-4	journal	September 2020
Coccolithovirus facilitation of carbon export in the North Atlantic Laber, Christien P.; Hunter, Jonathan E.; Carvalho, Filipa Nature Microbiology, Vol. 3, Issue 5 https://doi.org/10.1038/s41564-018-0128-4	journal	March 2018
Gpa, a Calcium-Binding Protein in the Coccolithophorid Emiliania Huxleyi (Prymnesiophyceae) Corstjens, Paul L. A. M.; van der Kooij, Annemieke; Linschooten, Cornelis Journal of Phycology, Vol. 34, Issue 4 https://doi.org/10.1046/j.1529-8817.1998.340622.x	journal	August 1998
ISOLATION AND CHARACTERIZATION OF A VIRUS THAT INFECTS EMILIANIA HUXLEYI (HAPTOPHYTA) ¹ Castberg, Tonje; Thyrhaug, Runar; Larsen, Aud Journal of Phycology, Vol. 38, Issue 4 https://doi.org/10.1046/j.1529-8817.2002.02015.x	journal	August 2002
Predominance of heavily calcified coccolithophores at low CaCO ₃ saturation during winter in the Bay of Biscay Smith, Helen E. K.; Tyrrell, Toby; Charalampopoulou, Anastasia Proceedings of the National Academy of Sciences, Vol. 109, Issue 23 https://doi.org/10.1073/pnas.1117508109	journal	May 2012
Host-virus dynamics and subcellular controls of cell fate in a natural coccolithophore population Vardi, A.; Haramaty, L.; Van Mooy, B. A. S. Proceedings of the National Academy of Sciences, Vol. 109, Issue 47 https://doi.org/10.1073/pnas.1208895109	journal	November 2012
Molecular Mechanisms Underlying Calcification in Coccolithophores Mackinder, Luke; Wheeler, Glen; Schroeder, Declan Geomicrobiology Journal, Vol. 27, Issue 6-7 https://doi.org/10.1080/01490451003703014	journal	September 2010
Dynamics of formation and secretion of heterococcoliths by *Coccolithus pelagicus* ssp. *braarudii* Taylor, Alison R.; Russell, Mark A.; Harper, Glenn M. European Journal of Phycology, Vol. 42, Issue 2 https://doi.org/10.1080/09670260601159346	journal	May 2007
Scalable Visualization Methods for Modern Generalized Additive Models Fasiolo, Matteo; Nedellec, Raphaël; Goude, Yannig Journal of Computational and Graphical Statistics, Vol. 29, Issue 1 https://doi.org/10.1080/10618600.2019.1629942	journal	July 2019
Variable production of transparent exopolymeric particles by haploid and diploid life stages of coccolithophores grown under different CO2 concentrations Pedrotti, M. L.; Fiorini, S.; Kerros, M. -E. Journal of Plankton Research, Vol. 34, Issue 5 https://doi.org/10.1093/plankt/fbs012	journal	March 2012
Calcification state of coccolithophores can be assessed by light scatter depolarization measurements with flow cytometry von Dassow, Peter; van den Engh, Ger; Iglesias-Rodriguez, Debora Journal of Plankton Research, Vol. 34, Issue 12 https://doi.org/10.1093/plankt/fbs061	journal	September 2012
A unicellular algal virus, Emiliania huxleyi virus 86, exploits an animal-like infection strategy Mackinder, L. C. M.; Worthy, C. A.; Biggi, G. Journal of General Virology, Vol. 90, Issue 9 https://doi.org/10.1099/vir.0.011635-0	journal	May 2009
The mutual interplay between calcification and coccolithovirus infection Johns, Christopher T.; Grubb, Austin R.; Nissimov, Jozef I. Environmental Microbiology, Vol. 21, Issue 6 https://doi.org/10.1111/1462-2920.14362	journal	September 2018
COCCOLITH PRODUCTION AND DETACHMENT BYEMILIANIA HUXLEYI(PRYMNESIOPHYCEAE)¹ Balch, William M.; Kilpatrick, Katherine; Holligan, Patrick M. Journal of Phycology, Vol. 29, Issue 5 https://doi.org/10.1111/j.0022-3646.1993.00566.x	journal	October 1993
In situ survey of life cycle phases of the coccolithophore Emiliania huxleyi (Haptophyta): Emiliania huxleyi life cycling Frada, Miguel J.; Bidle, Kay D.; Probert, Ian Environmental Microbiology, Vol. 14, Issue 6 https://doi.org/10.1111/j.1462-2920.2012.02745.x	journal	April 2012
Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models: Estimation of Semiparametric Generalized Linear Models Wood, Simon N. Journal of the Royal Statistical Society: Series B (Statistical Methodology), Vol. 73, Issue 1 https://doi.org/10.1111/j.1467-9868.2010.00749.x	journal	September 2010
NEW EVIDENCE FOR MORPHOLOGICAL AND GENETIC VARIATION IN THE COSMOPOLITAN COCCOLITHOPHORE EMILIANIA HUXLEYI (PRYMNESIOPHYCEAE) FROM THE COX1b-ATP4 GENES1: COX1-ATP4 GENES IN EMILIANIA HUXLEYI Hagino, Kyoko; Bendif, El Mahdi; Young, Jeremy R. Journal of Phycology, Vol. 47, Issue 5 https://doi.org/10.1111/j.1529-8817.2011.01053.x	journal	September 2011
phytools: an R package for phylogenetic comparative biology (and other things): phytools: R package Revell, Liam J. Methods in Ecology and Evolution, Vol. 3, Issue 2 https://doi.org/10.1111/j.2041-210X.2011.00169.x	journal	December 2011
The requirement for calcification differs between ecologically important coccolithophore species Walker, Charlotte E.; Taylor, Alison R.; Langer, Gerald New Phytologist, Vol. 220, Issue 1 https://doi.org/10.1111/nph.15272	journal	June 2018
Why marine phytoplankton calcify Monteiro, Fanny M.; Bach, Lennart T.; Brownlee, Colin Science Advances, Vol. 2, Issue 7 https://doi.org/10.1126/sciadv.1501822	journal	July 2016
Macromolecular recognition directs calcium ions to coccolith mineralization sites Gal, Assaf; Wirth, Richard; Kopka, Joachim Science, Vol. 353, Issue 6299 https://doi.org/10.1126/science.aaf7889	journal	August 2016
Optimization of Procedures for Counting Viruses by Flow Cytometry Brussaard, C. P. D. Applied and Environmental Microbiology, Vol. 70, Issue 3 https://doi.org/10.1128/AEM.70.3.1506-1513.2004	journal	March 2004
Particle Aggregation Burd, Adrian B.; Jackson, George A. Annual Review of Marine Science, Vol. 1, Issue 1 https://doi.org/10.1146/annurev.marine.010908.163904	journal	January 2009
Stable and Efficient Multiple Smoothing Parameter Estimation for Generalized Additive Models Wood, Simon N. Journal of the American Statistical Association, Vol. 99, Issue 467 https://doi.org/10.1198/016214504000000980	journal	September 2004
Generalized Additive Models Wood, Simon N. Chapman and Hall/CRC https://doi.org/10.1201/9781315370279	book	May 2017
Light scattering by coccoliths detached from Emiliania huxleyi Gordon, Howard R.; Smyth, Timothy J.; Balch, William M. Applied Optics, Vol. 48, Issue 31 https://doi.org/10.1364/AO.48.006059	journal	October 2009
Phenotypic Variability in the Coccolithophore Emiliania huxleyi Blanco-Ameijeiras, Sonia; Lebrato, Mario; Stoll, Heather M. PLOS ONE, Vol. 11, Issue 6 https://doi.org/10.1371/journal.pone.0157697	journal	June 2016
Intraspecific Differences in Biogeochemical Responses to Thermal Change in the Coccolithophore Emiliania huxleyi Matson, Paul G.; Ladd, Tanika M.; Halewood, Elisa R. PLOS ONE, Vol. 11, Issue 9 https://doi.org/10.1371/journal.pone.0162313	journal	September 2016
Emiliania huxleyi coccolith calcite mass modulation by morphological changes and ecology in the Mediterranean Sea D’Amario, Barbara; Ziveri, Patrizia; Grelaud, Michaël PLOS ONE, Vol. 13, Issue 7 https://doi.org/10.1371/journal.pone.0201161	journal	July 2018
A review of the coccolithophorid Emiliania huxleyi (Prymnesiophyceae), with particular reference to growth, coccolith formation, and calcification-photosynthesis interactions Paasche, E. Phycologia, Vol. 40, Issue 6 https://doi.org/10.2216/i0031-8884-40-6-503.1	journal	November 2001
Flow cytometric analysis of an Emiliana huxleyi bloom terminated by viral infection Jacquet, S.; Heldal, M.; Iglesias-Rodriguez, D. Aquatic Microbial Ecology, Vol. 27 https://doi.org/10.3354/ame027111	journal	January 2002
Viral mortality of the marine alga Emiliania huxleyi (Haptophyceae) and termination of algal blooms Bratbak, G.; Egge, Jk; Heldal, M. Marine Ecology Progress Series, Vol. 93 https://doi.org/10.3354/meps093039	journal	January 1993
Biometry of detached Emiliania huxleyi coccoliths along the Patagonian Shelf Poulton, Aj; Young, Jr; Bates, Nr Marine Ecology Progress Series, Vol. 443 https://doi.org/10.3354/meps09445	journal	December 2011
Photoacclimation to abrupt changes in light intensity by Phaeodactylum tricornutum and Emiliania huxleyi: the role of calcification Barcelos e. Ramos, J.; Schulz, Kg; Febiri, S. Marine Ecology Progress Series, Vol. 452 https://doi.org/10.3354/meps09606	journal	April 2012
Planktivorous feeding in calm and turbulent environments, with emphasis on copepods Kiørboe, T.; Saiz, E. Marine Ecology Progress Series, Vol. 122 https://doi.org/10.3354/meps122135	journal	January 1995
Exposure to oil from the 2015 Refugio spill alters the physiology of a common harmful algal bloom species, Pseudo-nitzschia australis, and the ubiquitous coccolithophore, Emiliania huxleyi Ladd, Tm; Bullington, Ja; Matson, Pg Marine Ecology Progress Series, Vol. 603 https://doi.org/10.3354/meps12710	journal	September 2018
An Extracellular Polysaccharide-Rich Organic Layer Contributes to Organization of the Coccosphere in Coccolithophores Walker, Charlotte E.; Heath, Sarah; Salmon, Deborah L. Frontiers in Marine Science, Vol. 5 https://doi.org/10.3389/fmars.2018.00306	journal	August 2018
Calcein Staining as a Tool to Investigate Coccolithophore Calcification Fox, Emily; Meyer, Erin; Panasiak, Natalie Frontiers in Marine Science, Vol. 5 https://doi.org/10.3389/fmars.2018.00326	journal	September 2018
Biological and optical properties of mesoscale coccolithophore blooms in the Gulf of Maine Balch, William M.; Holligan, Patrick M.; Ackleson, Steven G. Limnology and Oceanography, Vol. 36, Issue 4 https://doi.org/10.4319/lo.1991.36.4.0629	journal	June 1991
The role of coccoliths in protecting Emiliania huxleyi against stressful light and UV radiation Xu, Juntian; Bach, Lennart T.; Schulz, Kai G. Biogeosciences, Vol. 13, Issue 16 https://doi.org/10.5194/bg-13-4637-2016	journal	August 2016
Technical note: A refinement of coccolith separation methods: measuring the sinking characteristics of coccoliths Zhang, Hongrui; Stoll, Heather; Bolton, Clara Biogeosciences, Vol. 15, Issue 15 https://doi.org/10.5194/bg-15-4759-2018	journal	August 2018
Xenospheres and anomalous coccospheres from plankton samples of the Southern Indian Ocean. Patil, Sm.; Mohan, R.; Jafar, S. A. Journal of Nannoplankton Research, Vol. 36, Issue 2 https://doi.org/10.58998/jnr2189	journal	January 2016
Xenospheres – associations of coccoliths resembling coccospheres. Young, J. R.; Geisen, M. Journal of Nannoplankton Research, Vol. 24, Issue 1 https://doi.org/10.58998/jnr2283	journal	January 2002

Similar Records

Effect of viral infection on the ice nucleation efficiency of marine coccolithophores

Journal Article · Thu Nov 21 23:00:00 EST 2024 · Aerosol Science and Technology · OSTI ID:2480008

Magneto-optical properties of biogenic photonic crystals in algae

Journal Article · Wed May 07 00:00:00 EDT 2014 · Journal of Applied Physics · OSTI ID:22273920

Genome Variations Associated with Viral Susceptibility and Calcification in Emiliania huxleyi

Journal Article · Mon Nov 18 23:00:00 EST 2013 · PLoS ONE · OSTI ID:1627660

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Adsorptive exchange of coccolith biominerals facilitates viral infection

Citation Formats

References (63)

Similar Records

Related Subjects