Jump to ContentJump to Main Navigation
Show Summary Details
More options …

Botanica Marina

Editor-in-Chief: Dring, Matthew J.

IMPACT FACTOR 2018: 0.919
5-year IMPACT FACTOR: 1.336

CiteScore 2018: 1.22

SCImago Journal Rank (SJR) 2018: 0.399
Source Normalized Impact per Paper (SNIP) 2018: 0.672

See all formats and pricing
More options …
Ahead of print


Isolate-specific resistance to the algicidal bacterium Kordia algicida in the diatom Chaetoceros genus

Nils Meyer
  • Institute for Inorganic and Analytical Chemistry, Bioorganic Analytics, Friedrich Schiller University Jena, Lessingstrasse 8, D-07743 Jena, Germany
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Georg Pohnert
  • Corresponding author
  • Institute for Inorganic and Analytical Chemistry, Bioorganic Analytics, Friedrich Schiller University Jena, Lessingstrasse 8, D-07743 Jena, Germany
  • Max Planck Institute for Chemical Ecology, Hans Knöll Str. 8, D-07745 Jena, Germany
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2019-08-14 | DOI: https://doi.org/10.1515/bot-2019-0007


Algicidal bacteria can lyse phytoplankton cells, thereby contributing to algal bloom dynamics in the oceans. The target specificity of these bacteria determines their ecological impact. While species specificity of algicidal bacteria is documented, little is known about intra-species variability of their activity against phytoplankton. We describe variability in the Chaetoceros genus (Bacillariophyceae) to resist the lytic activity of the algicidal Flavobacterium Kordia algicida. This variability is evident between different Chaetoceros species, but even intra-specific variability of resistance is observed within one phytoplankton sample. This proves an ecological role of the individuality of diatom cells within a bloom.

Keywords: algicidal bacteria; diatoms; plankton; resistance; strain specificity


  • Ajani, P.A., T. Kahlke, N. Siboni, R. Carney, S.A. Murray and J.R. Seymour. 2018. The microbiome of the cosmopolitan diatom Leptocylindrus reveals significant spatial and temporal variability. Front. Microbiol. 9: 2758.CrossrefGoogle Scholar

  • Amin, S.A., M.S. Parker and E.V. Armbrust. 2012. Interactions between diatoms and bacteria. Microbiol. Mol. Biol. Rev. 76: 667–684.CrossrefGoogle Scholar

  • Behrenfeld, M.J., R.T. O’Malley, D.A. Siegel, C.R. McClain, J.L. Sarmiento, G.C. Feldman, A.J. Milligan, P.G. Falkowski, R.M. Letelier and E.S. Boss. 2006. Climate-driven trends in contemporary ocean productivity. Nature 444: 752–755.CrossrefGoogle Scholar

  • Bidle, K.D. and A. Vardi. 2011. A chemical arms race at sea mediates algal host-virus interactions. Curr. Opin. Microbiol. 14: 449–457.CrossrefGoogle Scholar

  • Bigalke, A., N. Meyer, L. Papanikolopoulou, K.H. Wiltshire and G. Pohnert. 2019. The algicidal bacterium Kordia algicida shapes a natural plankton community. Appl. Environ. Microb. 85: e02779–18.Google Scholar

  • Bolch, C.J.S., S.I. Blackburn, G.M. Hallegraeff and R.E. Vaillancourt. 1999. Genetic variation among strains of the toxic dinoflagellate Gymnodinium catenatum (Dinophyceae). J. Phycol. 35: 356–367.CrossrefGoogle Scholar

  • Brussaard, C.P.D. and J. Martínez-Martínez. 2008. Algal bloom viruses. Plant Viruses 2: 1–13.Google Scholar

  • Brussaard, C.P.D., R.S. Kempers, A.J. Kop, R. Riegman and M. Heldal. 1996. Virus-like particles in a summer bloom of Emiliania huxleyi in the North Sea. Aquat. Microb. Ecol. 10: 105–113.CrossrefGoogle Scholar

  • Desbois, A.P., M. Walton and V.J. Smith. 2010. Differential antibacterial activities of fusiform and oval morphotypes of Phaeodactylum tricornutum (Bacillariophyceae). J. Mar. Biol. Assoc. UK 90: 769–774.CrossrefGoogle Scholar

  • Frada, M., I. Probert, M.J. Allen, W.H. Wilson and C. de Vargas. 2008. The “Cheshire Cat” escape strategy of the coccolithophore Emiliania huxleyi in response to viral infection. Proc. Natl. Acad. Sci. U.S.A. 105: 15944–15949.CrossrefGoogle Scholar

  • Fredrickson, K.A., S.L. Strom, R. Crim and K.J. Coyne. 2011. Interstrain variability in physiology and genetics of Heterosigma Akashiwo (Raphidophyceae) from the west coast of North America. J. Phycol. 47: 25–35.CrossrefGoogle Scholar

  • French, F.W. and P.E. Hargraves. 1985. Spore formation in the life cycles of the diatoms Chaetoceros diadema and Leptocylindrus danicus. J. Phycol. 31: 477–483.Google Scholar

  • Gachon, C.M.M., T. Sime-Ngando, M. Strittmatter, A. Chambouvet and G.H. Kim. 2010. Algal diseases: spotlight on a black box. Trends Plant Sci. 15: 633–640.CrossrefGoogle Scholar

  • Garvette, A., E. Nezan, Y. Badis, G. Bilien, P. Arce, E. Bresnan, C.M.M. Gachon and R. Siano. 2018. Novel widespread marine oomycetes parasitising diatoms, including the toxic genus Pseudo-nitzschia: genetic, morphological, and ecological characterisation. Front. Microbiol. 9: 2918.CrossrefGoogle Scholar

  • Gladfelter, A.S., T.Y. James and A.S. Amend. 2019. Marine fungi. Curr. Biol. 29: R191–R195.CrossrefGoogle Scholar

  • Gleason, F.H., F.C. Kuepper, J.P. Amon, K. Picard, C.M.M. Gachon, A.V. Marano, T. Sime-Ngando and O. Lilje. 2011. Zoosporic true fungi in marine ecosystems: a review. Mar. Freshwater Res. 62: 383–393.CrossrefGoogle Scholar

  • Gumbo, R.J., G. Ross and E.T. Cloete. 2008. Biological control of Microcystis dominated harmful algal blooms. Afr. J. Biotechnol. 7: 4765–4773.Google Scholar

  • Hall, T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids Symp. Ser. 41: 95–98.Google Scholar

  • Hanic, L.A., S. Sekimoto and S.S. Bates. 2009. Oomycete and chytrid infections of the marine diatom Pseudo-nitzschia pungens (Bacillariophyceae) from Prince Edward Island, Canada. Botany 87: 1096–1105.CrossrefGoogle Scholar

  • Harvey, E.L., S. Menden-Deuer and T.A. Rynearson. 2015. Persistent intra-specific variation in genetic and behavioral traits in the Raphidophyte Heterosigma akashiwo. Front. Microbiol. 6: 1277.Google Scholar

  • Heil, C.A., P.M. Glibert and C.L. Fan. 2005. Prorocentrum minimum (Pavillard) Schiller – a review of a harmful algal bloom species of growing worldwide importance. Harmful Algae 4: 449–470.Google Scholar

  • Ibelings, B.W., A. De Bruin, M. Kagami, M. Rijkeboer, M. Brehm and E. van Donk. 2004. Host parasite interactions between freshwater phytoplankton and chytrid fungi (Chytridiomycota). J. Phycol. 40: 437–453.CrossrefGoogle Scholar

  • Jacobsen, A., A. Larsen, J. Martinez-Martinez, P.G. Verity and M.E. Frischer. 2007. Susceptibility of colonies and colonial cells of Phaeocystis pouchetii (Haptophyta) to viral infection. Aquat. Microb. Ecol. 48: 105–112.CrossrefGoogle Scholar

  • Jacquet, S., M. Heldal, D. Iglesias-Rodriguez, A. Larsen, W. Wilson and G. Bratbak. 2002. Flow cytometric analysis of an Emiliana huxleyi bloom terminated by viral infection. Aquat. Microb. Ecol. 27: 111–124.CrossrefGoogle Scholar

  • Kremp, A., A. Godhe, J. Egardt, S. Dupont, S. Suikkanen, S. Casabianca and A. Penna. 2012. Intraspecific variability in the response of bloom-forming marine microalgae to changed climate conditions. Ecol. Evol. 2: 1195–1207.CrossrefGoogle Scholar

  • Kumar, S., G. Stecher and K. Tamura. 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33: 1870–1874.CrossrefGoogle Scholar

  • Laurion, I. and S. Roy. 2009. Growth and photoprotection in three Dinoflagellates (including two strains of Alexandrium tamarense) and one diatom exposed to four weeks of natural and enhanced ultraviolet-B radiation. J. Phycol. 45: 16–33.CrossrefGoogle Scholar

  • Li, Y., S.Y. Zhu, N. Lundholm and S.H. Lu. 2015. Morphology and molecular phylogeny of Chaetoceros dayaensis sp. nov. (Bacillariophyceae), characterized by two 90 degrees rotations of the resting spore during maturation. J. Phycol. 51: 469–479.CrossrefGoogle Scholar

  • Loret, P., T. Tengs, T.A. Villareal, H. Singler, B. Richardson, P. McGuire, S. Morton, M. Busman and L. Campbell. 2002. No difference found in ribosomal DNA sequences from physiologically diverse clones of Karenia brevis (Dinophyceae) from the Gulf of Mexico. J. Plankton Res. 24: 735–739.CrossrefGoogle Scholar

  • Lundholm, N., N. Daugbjerg and O. Moestrup. 2002. Phylogeny of the Bacillariaceae with emphasis on the genus Pseudo-nitzschia (Bacillariophyceae) based on partial LSU rDNA. Eur. J. Phycol. 37: 115–134.CrossrefGoogle Scholar

  • Maier, I. and M. Calenberg. 1994. Effect of extracellular Ca2+ and Ca2+-antagonists on the movement and chemoorientation of male gametes of Ectocarpus siliculosus (Phaeophyceae). Bot. Acta 107: 451–460.CrossrefGoogle Scholar

  • Mayali, X. and G.J. Doucette. 2002. Microbial community interactions and population dynamics of an algicidal bacterium active against Karenia brevis (Dinophyceae). Harmful Algae 1: 277–293.CrossrefGoogle Scholar

  • McQuoid, M.R. and L.A. Hobson. 1996. Diatom resting stages. J. Phycol. 32: 889–902.CrossrefGoogle Scholar

  • Medlin, L.K., G.L.A. Barker, L. Campbell, J.C. Green, P.K. Hayes, D. Marie, S. Wrieden and D. Vaulot. 1996. Genetic characterisation of Emiliania huxleyi (Haptophyta). J. Marine Syst. 9: 13–31.CrossrefGoogle Scholar

  • Medlin, L.K., M. Lange and E.M. Nothig. 2000. Genetic diversity in the marine phytoplankton: a review and a consideration of Antarctic phytoplankton. Antarct. Sci. 12: 325–333.CrossrefGoogle Scholar

  • Menden-Deuer, S. and A.L. Montalbano. 2015. Bloom formation potential in the harmful dinoflagellate Akashiwo sanguinea: clues from movement behaviors and growth characteristics. Harmful Algae 47: 75–85.CrossrefGoogle Scholar

  • Meyer, N., A. Bigalke, A. Kaulfuss and G. Pohnert. 2017. Strategies and ecological roles of algicidal bacteria. Fems Microbiol. Rev. 41: 880–899.CrossrefGoogle Scholar

  • Meyer, N., J. Rettner, M. Werner, O. Werz and G. Pohnert. 2018. Algal oxylipins mediate the resistance of diatoms against algicidal bacteria. Mar. Drugs 16. doi: 10.3390/md16120486.Google Scholar

  • Mitsutani, A., K. Takesue, M. Kirita and Y. Ishida. 1992. Lysis of Skeletonema costatum by Cytophaga sp. isolated from the coastal water of the Ariake Sea. Nippon Suisan Gakk. 58: 2159–2167.CrossrefGoogle Scholar

  • Nunn, G.B., B.F. Theisen, B. Christensen and P. Arctander. 1996. Simplicity-correlated size growth of the nuclear 28S ribosomal RNA D3 expansion segment in the crustacean order Isopoda. J. Mol. Evol. 42: 211–223.CrossrefGoogle Scholar

  • Paul, C. and G. Pohnert. 2011. Interactions of the algicidal bacterium Kordia algicida with diatoms: regulated protease excretion for specific algal lysis. PLoS One 6: e21032.CrossrefGoogle Scholar

  • Paul, C. and G. Pohnert. 2013. Induction of protease release of the resistant diatom Chaetoceros didymus in response to lytic enzymes from an algicidal bacterium. PLoS One 8: e57577.CrossrefGoogle Scholar

  • Peacock, E.E., R.J. Olson and H.M. Sosik. 2014. Parasitic infection of the diatom Guinardia delicatula, a recurrent and ecologically important phenomenon on the New England Shelf. Mar. Ecol. Prog. Ser. 503: 1–10.CrossrefGoogle Scholar

  • Richards, T.A., M.D.M. Jones, G. Leonard and D. Bass. 2012. Marine fungi: their ecology and molecular diversity. Annu. Rev. Mar. Sci. 4: 495–522.CrossrefGoogle Scholar

  • Rodriguez, I., A. Alfonso, E. Alonso, J.A. Rubiolo, M. Roel, A. Vlamis, P. Katikou, S.A. Jackson, M.L. Menon, A. Dobson and L.M. Botana. 2017. The association of bacterial C-9-based TTX-like compounds with Prorocentrum minimum opens new uncertainties about shellfish seafood safety. Sci. Rep. 7: 40880.CrossrefGoogle Scholar

  • Rohwer, F. and R.V. Thurber. 2009. Viruses manipulate the marine environment. Nature 459: 207–212.CrossrefGoogle Scholar

  • Rosenwasser, S., C. Ziv, S.G. Van Creveld and A. Vardi. 2016. Virocell metabolism: metabolic innovations during host-virus interactions in the Ocean. Trends Microbiol. 24: 821–832.CrossrefGoogle Scholar

  • Roth, P.B., C.M. Mikulskil and G.J. Doucette. 2008a. Influence of microbial interactions on the susceptibility of Karenia spp. to algicidal bacteria. Aquat. Microb. Ecol. 50: 251–259.CrossrefGoogle Scholar

  • Roth, P.B., M.J. Twiner, C.M. Mikulski, A.B. Barnhorst and G.J. Doucette. 2008b. Comparative analysis of two algicidal bacteria active against the red tide dinoflagellate Karenia brevis. Harmful Algae 7: 682–691.CrossrefGoogle Scholar

  • Rynearson, T.A. and E.V. Armbrust. 2000. DNA fingerprinting reveals extensive genetic diversity in a field population of the centric diatom Ditylum brightwellii. Limnol. Oceanogr. 45: 1329–1340.CrossrefGoogle Scholar

  • Scholin, C.A., M.C. Villac, K.R. Buck, J.M. Krupp, D.A. Powers, G.A. Fryxell and F.P. Chavez. 1994. Ribosomal DNA sequences discriminate among toxic and non-toxic Pseudonitzschia species. Nat. Toxins 2: 152–165.CrossrefGoogle Scholar

  • Schroeder, D.C., J. Oke, G. Malin and W.H. Wilson. 2002. Coccolithovirus (Phycodnaviridae): Characterisation of a new large dsDNA algal virus that infects Emiliana huxleyi. Arch. Virol. 147: 1685–1698.CrossrefGoogle Scholar

  • Schroeder, D.C., J. Oke, M. Hall, G. Malin and W.H. Wilson. 2003. Virus succession observed during an Emiliania huxleyi bloom. Appl. Environ. Microb. 69: 2484–2490.CrossrefGoogle Scholar

  • Seong, K.A. and H.J. Jeong. 2013. Interactions between marine bacteria and red tide organisms in Korean waters. Algae-Seoul 28: 297–305.CrossrefGoogle Scholar

  • Seymour, J.R., S.A. Amin, J.B. Raina and R. Stocker. 2017. Zooming in on the phycosphere: the ecological interface for phytoplankton-bacteria relationships. Nat. Microbiol. 2: 17065.CrossrefGoogle Scholar

  • Shao, J.H., R.H. Li, J.E. Lepo and J.D. Gu. 2013. Potential for control of harmful cyanobacterial blooms using biologically derived substances: problems and prospects. J. Environ. Manage. 125: 149–155.CrossrefGoogle Scholar

  • Siano, R., C. Alves-de-Souza, E. Foulon, E.M. Bendif, N. Simon, L. Guillou and F. Not. 2011. Distribution and host diversity of Amoebophryidae parasites across oligotrophic waters of the Mediterranean Sea. Biogeosciences 8: 267–278.CrossrefGoogle Scholar

  • Sohn, J.H., J.H. Lee, H. Yi, J. Chun, K.S. Bae, T.Y. Ahn and S.J. Kim. 2004. Kordia algicida gen. nov., sp nov., an algicidal bacterium isolated from red tide. Int. J. Syst. Evol. Micr. 54: 675–680.CrossrefGoogle Scholar

  • Sparrow, F.K. 1969. Zoosporic marine fungi from the Pacific Northwest (U.S.A.). Arch. Mikrobiol. 66: 129–146.CrossrefGoogle Scholar

  • Tamura, K. and M. Nei. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial-DNA in humans and chimpanzees. Mol. Biol. Evol. 10: 512–526.Google Scholar

  • Taylor, R.L., K. Abrahamsson, A. Godhe and S.A. Wangberg. 2009. Seasonal variability in polyunsaturated aldehyde production potential among strains of Skeletonema marinoi (Bacillariophyceae). J. Phycol. 45: 46–53.CrossrefGoogle Scholar

  • Thessen, A.E., H.A. Bowers and D.K. Stoecker. 2009. Intra- and interspecies differences in growth and toxicity of Pseudo-nitzschia while using different nitrogen sources. Harmful Algae 8: 792–810.CrossrefGoogle Scholar

  • Thompson, J.D., D.G. Higgins and T.J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673–4680.CrossrefGoogle Scholar

  • Tillmann, U., K.J. Hesse and A. Tillmann. 1999. Large-scale parasitic infection of diatoms in the Northfrisian Wadden Sea. J. Sea Res. 42: 255–261.CrossrefGoogle Scholar

  • van Tol, H.M., S.A. Amin and E.V. Armbrust. 2016. Ubiquitous marine bacterium inhibits diatom cell division. ISME J. 11: 31–42.Google Scholar

  • Wichard, T., S.A. Poulet, C. Halsband-Lenk, A. Albaina, R. Harris, D. Liu and G. Pohnert. 2005. Survey of the chemical defence potential of diatoms: Screening of fifty one species for α,β,γ,δ-unsaturated aldehydes. J. Chem. Ecol. 31: 949–958.CrossrefGoogle Scholar

About the article

Nils Meyer

Nils Meyer is a PhD researcher at the Institute for Inorganic and Analytical Chemistry, Friedrich Schiller University Jena. After obtaining a Master’s degree in Chemical Biology (University Jena) he joined the collaborative research center ChemBioSys to study the chemical interaction of phytoplankton and algicidal bacteria.

Georg Pohnert

In his PhD at the University of Bonn Georg Pohnert investigated the biosynthesis and function of algal pheromones. He then moved to Cornell University where he did a postdoc in biophysics. His independent research career started at the Max Planck Institute for Chemical Ecology where he focused on chemical interactions of micro- and macroalgae – a topic that is also his current research focus at the Friedrich Schiller University Jena where he holds a chair in Bioorganic Analytics.

Received: 2019-01-23

Accepted: 2019-07-05

Published Online: 2019-08-14

Funding Source: German Research Foundation

Award identifier / Grant number: CRC 1127 ChemBioSys

The authors acknowledge all trainers and participants of the course “Algal Biodiversity” at Ghent University in 2015, especially Pieter Vanormelingen, for support in diatom isolation. Wiebe Kooistra is acknowledged for providing the Chaetoceros didymus strain. The authors acknowledge financial support from the German Research Foundation (Funder Id: http://dx.doi.org/10.13039/501100001659) within the framework of the CRC 1127 ChemBioSys.

Citation Information: Botanica Marina, 20190007, ISSN (Online) 1437-4323, ISSN (Print) 0006-8055, DOI: https://doi.org/10.1515/bot-2019-0007.

Export Citation

©2019 Walter de Gruyter GmbH, Berlin/Boston.Get Permission

Comments (0)

Please log in or register to comment.
Log in