Genome Variations Associated with Viral Susceptibility and Calcification in Emiliania huxleyi

Kegel, Jessica U.; John, Uwe; Valentin, Klaus; Frickenhaus, Stephan

doi:10.1371/journal.pone.0080684

Title: Genome Variations Associated with Viral Susceptibility and Calcification in Emiliania huxleyi

Journal Article · Tue Nov 19 00:00:00 EST 2013 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0080684· OSTI ID:1627660

Kegel, Jessica U. ^[1]; John, Uwe ^[1]; Valentin, Klaus ^[1]; Frickenhaus, Stephan ^[2]

Alfred Wegener Institute for Polar- and Marine Research Bremerhaven (Germany)
Alfred Wegener Institute for Polar- and Marine Research Bremerhaven (Germany); Hochschule Bremerhaven, Biotechnology (Germany)

Emiliania huxleyi, a key player in the global carbon cycle is one of the best studied coccolithophores with respect to biogeochemical cycles, climatology, and host-virus interactions. Strains of E. huxleyi show phenotypic plasticity regarding growth behaviour, light-response, calcification, acidification, and virus susceptibility. This phenomenon is likely a consequence of genomic differences, or transcriptomic responses, to environmental conditions or threats such as viral infections. We used an E. huxleyi genome microarray based on the sequenced strain CCMP1516 (reference strain) to perform comparative genomic hybridizations (CGH) of 16 E. huxleyi strains of different geographic origin. We investigated the genomic diversity and plasticity and focused on the identification of genes related to virus susceptibility and coccolith production (calcification). Among the tested 31940 gene models a core genome of 14628 genes was identified by hybridization among 16 E. huxleyi strains. 224 probes were characterized as specific for the reference strain CCMP1516. Compared to the sequenced E. huxleyi strain CCMP1516 variation in gene content of up to 30 percent among strains was observed. Comparison of core and non-core transcripts sets in terms of annotated functions reveals a broad, almost equal functional coverage over all KOG-categories of both transcript sets within the whole annotated genome. Within the variable (non-core) genome we identified genes associated with virus susceptibility and calcification. Genes associated with virus susceptibility include a Bax inhibitor-1 protein, three LRR receptor-like protein kinases, and mitogen-activated protein kinase. Our list of transcripts associated with coccolith production will stimulate further research, e.g. by genetic manipulation. In particular, the V-type proton ATPase 16 kDa proteolipid subunit is proposed to be a plausible target gene for further calcification studies.

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Research Organization:: Joint Genome Institute (JGI), Berkeley, CA (United States)

Sponsoring Organization:: USDOE; Alfred Wegener Institute; Helmholtz Foundation Initiative in Earth and Environment; Marine Genomics Europe

Grant/Contract Number:: AC02-05CH11231; 505403

OSTI ID:: 1627660

Journal Information:: PLoS ONE, Vol. 8, Issue 11; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (86)

The strain concept in phytoplankton ecology Lakeman, Michael Boyd; von Dassow, Peter; Cattolico, Rose Ann Harmful Algae, Vol. 8, Issue 5 https://doi.org/10.1016/j.hal.2008.11.011	journal	June 2009
Isolation of viruses responsible for the demise of an Emiliania huxleyi bloom in the English Channel Wilson, William H.; Tarran, Glen A.; Schroeder, Declan Journal of the Marine Biological Association of the United Kingdom, Vol. 82, Issue 3 https://doi.org/10.1017/S002531540200560X	journal	June 2002
Calcification, photosynthesis and growth of the bloom-forming coccolithophore, Emiliania huxleyi Balch, William M.; Holligan, Patrick M.; Kilpatrick, Katherine A. Continental Shelf Research, Vol. 12, Issue 12 https://doi.org/10.1016/0278-4343(92)90059-S	journal	December 1992
Strain-specific responses of Emiliania huxleyi to changing seawater carbonate chemistry Langer, G.; Nehrke, G.; Probert, I. Biogeosciences, Vol. 6, Issue 11 https://doi.org/10.5194/bg-6-2637-2009	journal	January 2009
The microbial pan-genome Medini, Duccio; Donati, Claudio; Tettelin, Hervé Current Opinion in Genetics & Development, Vol. 15, Issue 6 https://doi.org/10.1016/j.gde.2005.09.006	journal	December 2005
The Pfam Protein Families Database Bateman, A. Nucleic Acids Research, Vol. 30, Issue 1 https://doi.org/10.1093/nar/30.1.276	journal	January 2002
Biogeography of the Sulfolobus islandicus pan-genome Reno, M. L.; Held, N. L.; Fields, C. J. Proceedings of the National Academy of Sciences, Vol. 106, Issue 21 https://doi.org/10.1073/pnas.0808945106	journal	May 2009
Microarray estimation of genomic inter-strain variability in the genus Ectocarpus (Phaeophyceae) Dittami, Simon M.; Proux, Caroline; Rousvoal, Sylvie BMC Molecular Biology, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2199-12-2	journal	January 2011
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
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
A new approach to species determination for yeast strains: DNA microarray-based comparative genomic hybridization using a yeast DNA microarray with 6000 genes Watanabe, Takahito; Murata, Yoshinori; Oka, Syuichi Yeast, Vol. 21, Issue 4 https://doi.org/10.1002/yea.1103	journal	March 2004
Protein Kinase A-Dependent Step(s) in Hepatitis C Virus Entry and Infectivity Farquhar, Michelle J.; Harris, Helen J.; Diskar, Mandy Journal of Virology, Vol. 82, Issue 17 https://doi.org/10.1128/JVI.00592-08	journal	June 2008
CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Thompson, Julie D.; Higgins, Desmond G.; Gibson, Toby J. Nucleic Acids Research, Vol. 22, Issue 22, p. 4673-4680 https://doi.org/10.1093/nar/22.22.4673	journal	January 1994
Coccolithovirus (Phycodnaviridae): Characterisation of a new large dsDNA algal virus that infects Emiliana huxleyi Schroeder, D. C.; Oke, J.; Malin, G. Archives of Virology, Vol. 147, Issue 9 https://doi.org/10.1007/s00705-002-0841-3	journal	September 2002
Viral activation and recruitment of metacaspases in the unicellular coccolithophore, Emiliania huxleyi Bidle, K. D.; Haramaty, L.; Barcelos e. Ramos, J. Proceedings of the National Academy of Sciences, Vol. 104, Issue 14 https://doi.org/10.1073/pnas.0701240104	journal	March 2007
Analysis of Expressed Sequence Tags from Calcifying Cells of Marine Coccolithophorid (Emiliania huxleyi) Wahlund, ThomasM.; Hadaegh, AhmadR.; Clark, Robin Marine Biotechnology, Vol. 6, Issue 3 https://doi.org/10.1007/s10126-003-0035-3	journal	May 2004
Long Serial Analysis of Gene Expression for Gene Discovery and Transcriptome Profiling in the Widespread Marine Coccolithophore Emiliania huxleyi Dyhrman, S. T.; Haley, S. T.; Birkeland, S. R. Applied and Environmental Microbiology, Vol. 72, Issue 1 https://doi.org/10.1128/AEM.72.1.252-260.2006	journal	January 2006
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A. Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402 https://doi.org/10.1093/nar/25.17.3389	journal	September 1997
Satellite and ship studies of coccolithophore production along a continental shelf edge Holligan, P. M.; Viollier, M.; Harbour, D. S. Nature, Vol. 304, Issue 5924 https://doi.org/10.1038/304339a0	journal	July 1983
Molecular Dynamics of Emiliania huxleyi and Cooccurring Viruses during Two Separate Mesocosm Studies Martínez, Joaquín Martínez; Schroeder, Declan C.; Larsen, Aud Applied and Environmental Microbiology, Vol. 73, Issue 2 https://doi.org/10.1128/AEM.00864-06	journal	November 2006
Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: Implications for the microbial "pan-genome" Tettelin, H.; Masignani, V.; Cieslewicz, M. J. Proceedings of the National Academy of Sciences, Vol. 102, Issue 39 https://doi.org/10.1073/pnas.0506758102	journal	September 2005
A biogeochemical study of the coccolithophore, Emiliania huxleyi , in the North Atlantic Holligan, Patrick M.; Fernández, Emilio; Aiken, James Global Biogeochemical Cycles, Vol. 7, Issue 4 https://doi.org/10.1029/93GB01731	journal	December 1993
Regulation of Coccolith Calcification in Pleurochrysis carterae Marsh, Mary E. Handbook of Biomineralization: Biological Aspects and Structure Formation https://doi.org/10.1002/9783527619443.ch12	book	May 2007
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
Use of microarrays to assess viral diversity: from genotype to phenotype Allen, Michael J.; Martinez-Martinez, Joaquin; Schroeder, Declan C. Environmental Microbiology, Vol. 9, Issue 4 https://doi.org/10.1111/j.1462-2920.2006.01219.x	journal	April 2007
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
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
Interim Report on Genomics of Escherichia Coli Riley, M.; Serres, M. H. Annual Review of Microbiology, Vol. 54, Issue 1 https://doi.org/10.1146/annurev.micro.54.1.341	journal	October 2000
TM4: A Free, Open-Source System for Microarray Data Management and Analysis Saeed, A. I.; Sharov, V.; White, J. BioTechniques, Vol. 34, Issue 2 https://doi.org/10.2144/03342mt01	journal	February 2003
BAX INHIBITOR-1 Is Required for Full Susceptibility of Barley to Powdery Mildew Eichmann, Ruth; Bischof, Melanie; Weis, Corina Molecular Plant-Microbe Interactions®, Vol. 23, Issue 9 https://doi.org/10.1094/MPMI-23-9-1217	journal	September 2010
Genomic and Phenotypic Diversity of Coastal Vibrio cholerae Strains Is Linked to Environmental Factors Keymer, Daniel P.; Miller, Michael C.; Schoolnik, Gary K. Applied and Environmental Microbiology, Vol. 73, Issue 11 https://doi.org/10.1128/AEM.02736-06	journal	April 2007
Receptors and immune sensors: the complex entry path of human cytomegalovirus Compton, Teresa Trends in Cell Biology, Vol. 14, Issue 1 https://doi.org/10.1016/j.tcb.2003.10.009	journal	January 2004
Blooms of Emiliania huxleyi (Prymnesiophyceae) in surface waters of the Nova Scotian Shelf and the Grand Bank Brown, C. W.; Yoder, J. A. Journal of Plankton Research, Vol. 15, Issue 12 https://doi.org/10.1093/plankt/15.12.1429	journal	January 1993
Transcriptome Analyses Reveal Differential gene Expression Patterns Between the Life-Cycle Stages of Emiliania Huxleyi (Haptophyta) and Reflect Specialization to Different Ecological Niches1: gene Expression in e. Huxleyi Rokitta, Sebastian D.; de Nooijer, Lennart J.; Trimborn, Scarlett Journal of Phycology, Vol. 47, Issue 4 https://doi.org/10.1111/j.1529-8817.2011.01014.x	journal	July 2011
A model system approach to biological climate forcing. The example of Emiliania huxleyi Westbroek, Peter; Brown, Christopher W.; Bleijswijk, Judith van Global and Planetary Change, Vol. 8, Issue 1-2 https://doi.org/10.1016/0921-8181(93)90061-R	journal	July 1993
Ecological consequences of phenotypic plasticity Miner, Benjamin G.; Sultan, Sonia E.; Morgan, Steven G. Trends in Ecology & Evolution, Vol. 20, Issue 12 https://doi.org/10.1016/j.tree.2005.08.002	journal	December 2005
Evolution of Cell Recognition by Viruses Baranowski, E. Science, Vol. 292, Issue 5519 https://doi.org/10.1126/science.1058613	journal	May 2001
Resolution of a chronic viral infection after interleukin-10 receptor blockade Ejrnaes, Mette; Filippi, Christophe M.; Martinic, Marianne M. Journal of Experimental Medicine, Vol. 203, Issue 11 https://doi.org/10.1084/jem.20061462	journal	October 2006
A COCCOLITHOPHORID CALCIFYING VESICLE WITH A VACUOLAR-TYPE ATPASE PROTON PUMP: CLONING AND IMMUNOLOCALIZATION OF THE V0 SUBUNIT c Corstjens, Paul L. A. M.; Araki, Yoko; Gonzalez, Elma L. Journal of Phycology, Vol. 37, Issue 1 https://doi.org/10.1046/j.1529-8817.1999.014012071.x	journal	February 2001
Evolution of the core and pan-genome of Streptococcus: positive selection, recombination, and genome composition Lefébure, Tristan; Stanhope, Michael J. Genome Biology, Vol. 8, Issue 5 https://doi.org/10.1186/gb-2007-8-5-r71	journal	January 2007
Respiratory Syncytial Virus Infection Results in Activation of Multiple Protein Kinase C Isoforms Leading to Activation of Mitogen-Activated Protein Kinase Monick, Martha M.; Staber, Janice M.; Thomas, Karl W. The Journal of Immunology, Vol. 166, Issue 4 https://doi.org/10.4049/jimmunol.166.4.2681	journal	February 2001
A chemical arms race at sea mediates algal host–virus interactions Bidle, Kay D.; Vardi, Assaf Current Opinion in Microbiology, Vol. 14, Issue 4 https://doi.org/10.1016/j.mib.2011.07.013	journal	August 2011
CELL CYCLE DEPENDENT VIRUS PRODUCTION IN MARINE PHYTOPLANKTON ¹ Thyrhaug, Runar; Larsen, Aud; Brussaard, Corina P. D. Journal of Phycology, Vol. 38, Issue 2 https://doi.org/10.1046/j.1529-8817.2002.01154.x	journal	April 2002
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
Global synchroneity of late Quaternary coccolith datum levels Validation by oxygen isotopes Thierstein, H. R.; Geitzenauer, K. R.; Molfino, B. Geology, Vol. 5, Issue 7 https://doi.org/10.1130/0091-7613(1977)5<400:GSOLQC>2.0.CO;2	journal	January 1977
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
ASSESSING THE ROLE OF CASPASE ACTIVITY AND METACASPASE EXPRESSION ON VIRAL SUSCEPTIBILITY OF THE COCCOLITHOPHORE, EMILIANIA HUXLEYI (HAPTOPHYTA) Bidle, Kay D.; Kwityn, Clifford J. Journal of Phycology, Vol. 48, Issue 5 https://doi.org/10.1111/j.1529-8817.2012.01209.x	journal	August 2012
Complete Genome Sequence and Lytic Phase Transcription Profile of a Coccolithovirus Wilson, W. H. Science, Vol. 309, Issue 5737 https://doi.org/10.1126/science.1113109	journal	August 2005
The relative significance of viral lysis and microzooplankton grazing as pathways of dimethylsulfoniopropionate (DMSP) cleavage: An Emiliania huxleyi culture study Evans, Claire; Kadner, Susanne V.; Darroch, Louise J. Limnology and Oceanography, Vol. 52, Issue 3 https://doi.org/10.4319/lo.2007.52.3.1036	journal	May 2007
Genetic characterisation of Emiliania huxleyi (Haptophyta) Medlin, L. K.; Barker, G. L. A.; Campbell, L. Journal of Marine Systems, Vol. 9, Issue 1-2 https://doi.org/10.1016/0924-7963(96)00013-9	journal	October 1996
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
Polymorphic microsatellite loci in global populations of the marine coccolithophorid Emiliania huxleyi Iglesias-Rodriguez, M. Debora; Saez, Alberto G.; Groben, Rene Molecular Ecology Notes, Vol. 2, Issue 4 https://doi.org/10.1046/j.1471-8286.2002.00289.x	journal	December 2002
A novel highly acidic polysaccharide with inhibitory activity on calcification from the calcified scale “coccolith” of a coccolithophorid alga, Pleurochrysis haptonemofera Ozaki, Noriaki; Sakuda, Shohei; Nagasawa, Hiromichi Biochemical and Biophysical Research Communications, Vol. 357, Issue 4 https://doi.org/10.1016/j.bbrc.2007.04.078	journal	June 2007
Regulation of CaCO3 formation in coccolithophores Marsh, M. E. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, Vol. 136, Issue 4 https://doi.org/10.1016/S1096-4959(03)00180-5	journal	December 2003
cDNA Microarrays as a Tool for Identification of Biomineralization Proteins in the Coccolithophorid Emiliania huxleyi (Haptophyta) Quinn, Patrick; Bowers, Robert M.; Zhang, Xiaoyu Applied and Environmental Microbiology, Vol. 72, Issue 8 https://doi.org/10.1128/AEM.00343-06	journal	August 2006
APE: Analyses of Phylogenetics and Evolution in R language Paradis, E.; Claude, J.; Strimmer, K. Bioinformatics, Vol. 20, Issue 2 https://doi.org/10.1093/bioinformatics/btg412	journal	January 2004
Pan genome of the phytoplankton Emiliania underpins its global distribution Read, Betsy A.; Kegel, Jessica; Klute, Mary J. Nature, Vol. 499, Issue 7457 https://doi.org/10.1038/nature12221	journal	June 2013
Viral Infection of Emiliania Huxleyi (Prymnesiophyceae) Leads to Elevated Production of Reactive Oxygen Species Evans, Claire; Malin, Gillian; Mills, Graham P. Journal of Phycology, Vol. 42, Issue 5 https://doi.org/10.1111/j.1529-8817.2006.00256.x	journal	October 2006
Emiliania huxleyi shows identical responses to elevated pCO2 in TA and DIC manipulations Hoppe, C. J. M.; Langer, G.; Rost, B. Journal of Experimental Marine Biology and Ecology, Vol. 406, Issue 1-2 https://doi.org/10.1016/j.jembe.2011.06.008	journal	September 2011
Protein database searches using compositionally adjusted substitution matrices Altschul, Stephen F.; Wootton, John C.; Gertz, E. Michael FEBS Journal, Vol. 272, Issue 20 https://doi.org/10.1111/j.1742-4658.2005.04945.x	journal	October 2005
Overexpression of barley BAX inhibitor 1 induces breakdown of mlo-mediated penetration resistance to Blumeria graminis Huckelhoven, R.; Dechert, C.; Kogel, K. -H. Proceedings of the National Academy of Sciences, Vol. 100, Issue 9 https://doi.org/10.1073/pnas.0931464100	journal	April 2003
Extensive Genomic Diversity in Pathogenic Escherichia coli and Shigella Strains Revealed by Comparative Genomic Hybridization Microarray Fukiya, Satoru; Mizoguchi, Hiroshi; Tobe, Toru Journal of Bacteriology, Vol. 186, Issue 12 https://doi.org/10.1128/JB.186.12.3911-3921.2004	journal	June 2004
Viral Glycosphingolipids Induce Lytic Infection and Cell Death in Marine Phytoplankton Vardi, A.; Van Mooy, B. A. S.; Fredricks, H. F. Science, Vol. 326, Issue 5954 https://doi.org/10.1126/science.1177322	journal	November 2009
Evolutionary History of the Coccolithoviridae Allen, Michael J.; Schroeder, Declan C.; Holden, Matthew T. G. Molecular Biology and Evolution, Vol. 23, Issue 1 https://doi.org/10.1093/molbev/msj010	journal	September 2005
V- AND P-TYPE Ca2+-STIMULATED ATPases IN A CALCIFYING STRAIN OF PLEUROCHRYSIS SP. (HAPTOPHYCEAE) Araki, Yoko; Gonzalez, Elma L. Journal of Phycology, Vol. 34, Issue 1 https://doi.org/10.1046/j.1529-8817.1998.340079.x	journal	February 1998
Preliminary characterisation of repeat families in the genome of EhV-86, a giant algal virus that infects the marine microalga Emiliania huxleyi Allen, M. J.; Schroeder, D. C.; Wilson, W. H. Archives of Virology, Vol. 151, Issue 3 https://doi.org/10.1007/s00705-005-0647-1	journal	September 2005
Photosynthetic Pigment and Genetic Differences Between two Southern Ocean Morphotypes of Emiliania Huxleyi (Haptophyta)1: Emiliania Huxleyi Morphotypes Cook, Suellen S.; Whittock, Lucy; Wright, Simon W. Journal of Phycology, Vol. 47, Issue 3 https://doi.org/10.1111/j.1529-8817.2011.00992.x	journal	May 2011
Transgenic mice expressing a human poliovirus receptor: A new model for poliomyelitis Ren, Ruibao; Costantini, Frank; Gorgacz, Edward J. Cell, Vol. 63, Issue 2 https://doi.org/10.1016/0092-8674(90)90168-e	journal	October 1990
Comparative genome analysis of Campylobacter jejuni using whole genome DNA microarrays Pearson, B. M.; Pin, C.; Wright, J. FEBS Letters, Vol. 554, Issue 1-2 https://doi.org/10.1016/s0014-5793(03)01164-5	journal	October 2003
Structure, function and evolution of plant disease resistance genes Ellis, Jeff; Dodds, Peter; Pryor, Tony Current Opinion in Plant Biology, Vol. 3, Issue 4 https://doi.org/10.1016/s1369-5266(00)00080-7	journal	August 2000
BAX Inhibitor-1, an ancient cell death suppressor in animals and plants with prokaryotic relatives Hückelhoven, R. Apoptosis, Vol. 9, Issue 3 https://doi.org/10.1023/b:appt.0000025806.71000.1c	journal	May 2004
The vaccinia virus-stimulated mitogen-activated protein kinase (MAPK) pathway is required for virus multiplication Andrade, Anderson A.; Silva, Patrícia N. G.; Pereira, Anna C. T. C. Biochemical Journal, Vol. 381, Issue 2 https://doi.org/10.1042/bj20031375	journal	July 2004
Devil inside: does plant programmed cell death involve the endomembrane system? Cacas, Jean-Luc Plant, Cell & Environment https://doi.org/10.1111/j.1365-3040.2010.02117.x	journal	March 2010
Streptococcus thermophilus Core Genome: Comparative Genome Hybridization Study of 47 Strains Rasmussen, Thomas Bovbjerg; Danielsen, Morten; Valina, Ondrej Applied and Environmental Microbiology, Vol. 74, Issue 15 https://doi.org/10.1128/aem.00132-08	journal	June 2008
Identification and Preliminary Characterization of Two cDNAs Encoding Unique Carbonic Anhydrases from the Marine Alga Emiliania huxleyi Soto, Amelia R.; Zheng, Hong; Shoemaker, Dorinda Applied and Environmental Microbiology, Vol. 72, Issue 8 https://doi.org/10.1128/aem.00237-06	journal	August 2006
Light-Dependent Transcriptional Regulation of Genes of Biogeochemical Interest in the Diploid and Haploid Life Cycle Stages of Emiliania huxleyi Richier, Sophie; Kerros, Marie-Emmanuelle; de Vargas, Colomban Applied and Environmental Microbiology, Vol. 75, Issue 10 https://doi.org/10.1128/aem.02737-08	journal	March 2009
Virus Succession Observed during an Emiliania huxleyi Bloom Schroeder, Declan C.; Oke, Joanne; Hall, Matthew Applied and Environmental Microbiology, Vol. 69, Issue 5 https://doi.org/10.1128/aem.69.5.2484-2490.2003	journal	May 2003
Suppressive Subtractive Hybridization of and Differences in Gene Expression Content of Calcifying and Noncalcifying Cultures of Emiliania huxleyi Strain 1516 Nguyen, Binh; Bowers, Robert M.; Wahlund, Thomas M. Applied and Environmental Microbiology, Vol. 71, Issue 5 https://doi.org/10.1128/aem.71.5.2564-2575.2005	journal	May 2005
Virus receptors: implications for pathogenesis and the design of antiviral agents. Norkin, L. C. Clinical Microbiology Reviews, Vol. 8, Issue 2 https://doi.org/10.1128/cmr.8.2.293	journal	April 1995
Bacillus subtilis Genome Diversity Earl, Ashlee M.; Losick, Richard; Kolter, Roberto Journal of Bacteriology, Vol. 189, Issue 3 https://doi.org/10.1128/jb.01343-06	journal	November 2006
Toll-Like Receptor 4-Mediated Activation of p38 Mitogen-Activated Protein Kinase Is a Determinant of Respiratory Virus Entry and Tropism Marchant, David; Singhera, Gurpreet K.; Utokaparch, Soraya Journal of Virology, Vol. 84, Issue 21 https://doi.org/10.1128/jvi.00804-10	journal	August 2010
Selective receptor expression restricts Nipah virus infection of endothelial cells Erbar, Stephanie; Diederich, Sandra; Maisner, Andrea Virology Journal, Vol. 5, Issue 1 https://doi.org/10.1186/1743-422x-5-142	journal	January 2008
Transcriptome analysis of functional differentiation between haploid and diploid cells of Emiliania huxleyi, a globally significant photosynthetic calcifying cell von Dassow, Peter; Ogata, Hiroyuki; Probert, Ian Genome Biology, Vol. 10, Issue 10 https://doi.org/10.1186/gb-2009-10-10-r114	journal	January 2009
Learning from the Viral Journey: How to Enter Cells and How to Overcome Intracellular Barriers to Reach the Nucleus Mudhakir, Diky; Harashima, Hideyoshi The AAPS Journal, Vol. 11, Issue 1 https://doi.org/10.1208/s12248-009-9080-9	journal	February 2009
Mitogen-Activated Protein (MAP) Kinase Pathways: Regulation and Physiological Functions* Pearson, Gray; Robinson, Fred; Beers Gibson, Tara Endocrine Reviews, Vol. 22, Issue 2 https://doi.org/10.1210/edrv.22.2.0428	journal	April 2001
Effects of CO₂ and their modulation by light in the life-cycle stages of the coccolithophore Emiliania huxleyi Rokitta, Sebastian D.; Rost, Björn Limnology and Oceanography, Vol. 57, Issue 2 https://doi.org/10.4319/lo.2012.57.2.0607	journal	March 2012

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Correction: Ruiz, E. et al. Emerging Interaction Patterns in the Emiliania Huxleyi-EhV System. Viruses 2016, 9, 61 Ruiz, Eliana; Oosterhof, Monique; Sandaa, Ruth-Anne Viruses, Vol. 9, Issue 4 https://doi.org/10.3390/v9040089	journal	April 2017

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