Interactions between Diatoms and Bacteria

SUMMARY Diatoms and bacteria have cooccurred in common habitats for hundreds of millions of years, thus fostering specific associations and interactions with global biogeochemical consequences. Diatoms are responsible for one-fifth of the photosynthesis on Earth, while bacteria remineralize a large portion of this fixed carbon in the oceans. Through their coexistence, diatoms and bacteria cycle nutrients between oxidized and reduced states, impacting bioavailability and ultimately feeding higher trophic levels. Here we present an overview of how diatoms and bacteria interact and the implications of these interactions. We emphasize that heterotrophic bacteria in the oceans that are consistently associated with diatoms are confined to two phyla. These consistent bacterial associations result from encounter mechanisms that occur within a microscale environment surrounding a diatom cell. We review signaling mechanisms that occur in this microenvironment to pave the way for specific interactions. Finally, we discuss known interactions between diatoms and bacteria and exciting new directions and research opportunities in this field. Throughout the review, we emphasize new technological advances that will help in the discovery of new interactions. Deciphering the languages of diatoms and bacteria and how they interact will inform our understanding of the role these organisms have in shaping the ocean and how these interactions may change in future oceans.

[1]  T. Lebeau,et al.  Diatom cultivation and biotechnologically relevant products. Part II: Current and putative products , 2003, Applied Microbiology and Biotechnology.

[2]  Takeshi Terada,et al.  Carbon and nitrogen assimilation in deep subseafloor microbial cells , 2011, Proceedings of the National Academy of Sciences.

[3]  T. Oh,et al.  Winogradskyella aquimaris sp. nov., isolated from seawater. , 2012, International journal of systematic and evolutionary microbiology.

[4]  K. Denman,et al.  Phytoplankton patchiness indicates the fluctuation spectrum of mesoscale oceanic structure , 1980, Nature.

[5]  T. Sakata,et al.  Algicidal activity and gliding motility of Saprospira sp. SS98-5. , 2003, Canadian journal of microbiology.

[6]  F. Morel,et al.  Response of cell surface pH to pCO2 and iron limitation in the marine diatom Thalassiosira weissflogii , 2009 .

[7]  P. Karlson,et al.  ‘Pheromones’: a New Term for a Class of Biologically Active Substances , 1959, Nature.

[8]  S. Wakeham,et al.  Compositions and transport of lipid biomarkers through the water column and surficial sediments of the equatorial Pacific Ocean , 1997 .

[9]  V. Smetácek,et al.  Aldehyde suppression of copepod recruitment in blooms of a ubiquitous planktonic diatom , 2004, Nature.

[10]  F. T.,et al.  Phytoplankton-bacteria interactions : an apparent paradox ? Analysis of a model system with both competition and commensalism , 2006 .

[11]  D. J. Douglas,et al.  Biosynthesis of domoic acid by the diatom Pseudo-nitzschia multiseries. , 1998, Natural toxins.

[12]  William M. Durham,et al.  Disruption of Vertical Motility by Shear Triggers Formation of Thin Phytoplankton Layers , 2009, Science.

[13]  V. Sperandio,et al.  The QseC sensor kinase: A bacterial adrenergic receptor , 2006, Proceedings of the National Academy of Sciences.

[14]  James G. Mitchell,et al.  Bacterial tracking of motile algae. , 2003, FEMS microbiology ecology.

[15]  T. Mincer,et al.  Possible influence of bacterial quorum sensing on the hydrolysis of sinking particulate organic carbon in marine environments. , 2011, Environmental microbiology reports.

[16]  V. Trainer,et al.  Domoic acid: The synergy of iron, copper, and the toxicity of diatoms , 2005 .

[17]  Roslyn M. Theisen,et al.  Iron(III)-siderophore coordination chemistry: Reactivity of marine siderophores. , 2010, Coordination chemistry reviews.

[18]  Farooq Azam,et al.  Major role of bacteria in biogeochemical fluxes in the ocean's interior , 1988, Nature.

[19]  G. Bratbak,et al.  Phytoplankton-bacteria interactions: an apparant paradox? Analysis of a model system with both competition and commensalism , 1985 .

[20]  K. Rumbaugh Convergence of hormones and autoinducers at the host/pathogen interface , 2007, Analytical and bioanalytical chemistry.

[21]  W. Whitman,et al.  Prokaryotes: the unseen majority. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Jo Handelsman,et al.  Toward a Census of Bacteria in Soil , 2006, PLoS Comput. Biol..

[23]  E. Delong,et al.  The Microbial Engines That Drive Earth's Biogeochemical Cycles , 2008, Science.

[24]  M. C. Horner-Devine,et al.  Bacterial community composition differs with species and toxigenicity of the diatom Pseudo-nitzschia , 2011 .

[25]  T. Katano,et al.  Pseudomonas fluorescens HYK0210‐SK09 offers species‐specific biological control of winter algal blooms caused by freshwater diatom Stephanodiscus hantzschii , 2008, Journal of applied microbiology.

[26]  Chris Bowler,et al.  A Stress Surveillance System Based on Calcium and Nitric Oxide in Marine Diatoms , 2006, PLoS biology.

[27]  C. Carrano,et al.  Iron transport in the genus Marinobacter , 2012, BioMetals.

[28]  E. Allain,et al.  Reaction of Acylated Homoserine Lactone Bacterial Signaling Molecules with Oxidized Halogen Antimicrobials , 2001, Applied and Environmental Microbiology.

[29]  M. Moran,et al.  Bacterial community transcription patterns during a marine phytoplankton bloom. , 2012, Environmental microbiology.

[30]  J. Gavis,et al.  Transport limited nutrient uptake rates in Ditylum brightwellii1 , 1975 .

[31]  Christina Toft,et al.  Evolutionary microbial genomics: insights into bacterial host adaptation , 2010, Nature Reviews Genetics.

[32]  S. Lindow,et al.  Disruption of N-Αcyl Homoserine Lactone-Mediated Cell Signaling and Iron Acquisition in Epiphytic Bacteria by Leaf Surface Compounds , 2006, Applied and Environmental Microbiology.

[33]  S. Kjelleberg,et al.  Halogenated furanones from the red alga, Delisea pulchra, inhibit carbapenem antibiotic synthesis and exoenzyme virulence factor production in the phytopathogen Erwinia carotovora. , 2001, FEMS microbiology letters.

[34]  V. Smith,et al.  Differential antibacterial activities of fusiform and oval morphotypes of Phaeodactylum tricornutum (Bacillariophyceae) , 2010, Journal of the Marine Biological Association of the United Kingdom.

[35]  Morten Nielsen,et al.  CPHmodels-3.0—remote homology modeling using structure-guided sequence profiles , 2010, Nucleic Acids Res..

[36]  H. Grossart,et al.  Diatom-associated bacteria are required for aggregation of Thalassiosira weissflogii , 2011, The ISME Journal.

[37]  Maurizio Labbate,et al.  AHL-driven quorum-sensing circuits: their frequency and function among the Proteobacteria , 2008, The ISME Journal.

[38]  Natalia N. Ivanova,et al.  A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea , 2009, Nature.

[39]  J. Durner,et al.  Response of Arabidopsis thaliana to N-hexanoyl-dl-homoserine-lactone, a bacterial quorum sensing molecule produced in the rhizosphere , 2008, Planta.

[40]  Nicholas H. Putnam,et al.  The Genome of the Diatom Thalassiosira Pseudonana: Ecology, Evolution, and Metabolism , 2004, Science.

[41]  R. Cortese,et al.  The crystal structure of the quorum sensing protein TraR bound to its autoinducer and target DNA , 2002, The EMBO journal.

[42]  Roman Stocker,et al.  Rapid chemotactic response enables marine bacteria to exploit ephemeral microscale nutrient patches , 2008, Proceedings of the National Academy of Sciences.

[43]  Shawn R Campagna,et al.  Quorum sensing control of phosphorus acquisition in Trichodesmium consortia , 2011, The ISME Journal.

[44]  K. Nealson,et al.  Cellular Control of the Synthesis and Activity of the Bacterial Luminescent System , 1970, Journal of bacteriology.

[45]  Xi-Ying Zhang,et al.  Neptunomonas antarctica sp. nov., isolated from marine sediment. , 2010, International journal of systematic and evolutionary microbiology.

[46]  N. Taga,et al.  Distribution and seasonal variation of vitamin B12, thiamine and biotin in the sea , 1972 .

[47]  S. Rice,et al.  Inhibition of Luminescence and Virulence in the Black Tiger Prawn (Penaeus monodon) Pathogen Vibrio harveyi by Intercellular Signal Antagonists , 2000, Applied and Environmental Microbiology.

[48]  R. Sayre,et al.  N‐ACYL HOMOSERINE LACTONe LACTONASE, AiiA, INACTIVATION OF QUORUM‐SENSING AGONISTS PRODUCED BY CHLAMYDOMONAS REINHARDTII (CHLOROPHYTA) AND CHARACTERIZATION OF aiiA TRANSGENIC ALGAE 1 , 2011, Journal of phycology.

[49]  E. Virginia Armbrust,et al.  The life of diatoms in the world's oceans , 2009, Nature.

[50]  G. Doucette,et al.  Relationships Between Bacteria and Harmful Algae , 2006 .

[51]  U. Nantes Diatom cultivation and biotechnologically relevant products. Part II: Current and putative products , 2003 .

[52]  J. W. Wells,et al.  Interaction of domoic acid and several derivatives with kainic acid and AMPA binding sites in rat brain. , 1992, European journal of pharmacology.

[53]  F. Fang,et al.  NO inhibitions: antimicrobial properties of nitric oxide. , 1995, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[54]  K. Ohwada Seasonal Cycles of Vitamin B12, Thiamine and Biotin in Lake Sagami. Patterns of Their Distribution and Ecological Significance , 1973 .

[55]  Mitchell,et al.  Microscale nutrient patches in planktonic habitats shown by chemotactic bacteria , 1998, Science.

[56]  R. Reid,et al.  Autoinducers extracted from microbial mats reveal a surprising diversity of N-acylhomoserine lactones (AHLs) and abundance changes that may relate to diel pH. , 2009, Environmental microbiology.

[57]  M. Kuypers,et al.  Nitrogen fixation and transfer in open ocean diatom–cyanobacterial symbioses , 2011, The ISME Journal.

[58]  Ralph Mitchell,et al.  Studies in Bacterial Chemoreception. I. The Effect of Biogenic Amines and Cannabinoids on Bacterial Chemoreception. II. Chemotactic and Growth Responses of Marine Bacteria to Algal Extracellular Products. , 1972 .

[59]  A. Carlucci,et al.  EFFECT OF VITAMIN CONCENTRATIONS ON GROWTH AND DEVELOPMENT OF VITAMIN‐REQUIRING ALGAE 1 , 1969, Journal of phycology.

[60]  J. G. Mitchell,et al.  Clustering of marine bacteria in seawater enrichments , 1996, Applied and environmental microbiology.

[61]  K. Schleifer,et al.  Gelidibacter mesophilus sp. nov., a novel marine bacterium in the family Flavobacteriaceae. , 2002, International journal of systematic and evolutionary microbiology.

[62]  T. Sakata,et al.  Characterization and expression of Saprospira cytoplasmic fibril protein (SCFP) gene from algicidal Saprospira spp. strains , 2008, Fisheries Science.

[63]  C. Hassler,et al.  Saccharides enhance iron bioavailability to Southern Ocean phytoplankton , 2010, Proceedings of the National Academy of Sciences.

[64]  R. Casotti,et al.  Differential effect of three polyunsaturated aldehydes on marine bacterial isolates. , 2008, Aquatic toxicology.

[65]  J. Ehrman,et al.  Interaction between bacteria and the domoic-acid-producing diatom Pseudo-nitzschia multiseries (Hasle) Hasle; can bacteria produce domoic acid autonomously? , 2004 .

[66]  A. Wichels,et al.  Bacterial community dynamics during the winter-spring transition in the North Sea. , 2007, FEMS microbiology ecology.

[67]  Ulf Riebesell,et al.  Diffusion and reactions in the vicinity of plankton: A refined model for inorganic carbon transport , 1997 .

[68]  J. Stewart Bacterial involvement in determining domoic acid levels in Pseudo-nitzschia multiseries cultures , 2008 .

[69]  R. Armstrong Nutrient uptake rate as a function of cell size and surface transporter density: A Michaelis-like approximation to the model of Pasciak and Gavis , 2008 .

[70]  J. Komárek,et al.  Modern taxonomic revision of planktic nostocacean cyanobacteria: a short review of genera , 2010, Hydrobiologia.

[71]  A. Butler,et al.  Photoreactivity of iron(III)-aerobactin: photoproduct structure and iron(III) coordination. , 2006, Inorganic chemistry.

[72]  C. L. Burton,et al.  The Growth Response of Escherichia coli to Neurotransmitters and Related Catecholamine Drugs Requires a Functional Enterobactin Biosynthesis and Uptake System , 2002, Infection and Immunity.

[73]  E. Boss,et al.  Nutrient fluxes to planktonic osmotrophs in the presence of fluid motion , 1996 .

[74]  R. Blondeau,et al.  On the Iron Requirement of Lactobacilli Grown in Chemically Defined Medium , 1998, Current Microbiology.

[75]  E. Greenberg,et al.  Human and murine paraoxonase 1 are host modulators of Pseudomonas aeruginosa quorum-sensing. , 2005, FEMS microbiology letters.

[76]  Martin J. Warren,et al.  Algae acquire vitamin B12 through a symbiotic relationship with bacteria , 2005, Nature.

[77]  N. Revsbech,et al.  Competition between Ammonia-Oxidizing Bacteria and Benthic Microalgae , 2004, Applied and Environmental Microbiology.

[78]  S. Waksman,et al.  MARINE BACTERIA AND THEIR RÔLE IN THE CYCLE OF LIFE IN THE SEA I. DECOMPOSITION OF MARINE PLANT AND ANIMAL RESIDUES BY BACTERIA , 1933 .

[79]  E. Armbrust,et al.  Succession and Diel Transcriptional Response of the Glycolate-Utilizing Component of the Bacterial Community during a Spring Phytoplankton Bloom , 2007, Applied and Environmental Microbiology.

[80]  E. Armbrust,et al.  Detection of glycolate oxidase gene glcD diversity among cultured and environmental marine bacteria. , 2006, Environmental microbiology.

[81]  S. Strom Microbial Ecology of Ocean Biogeochemistry: A Community Perspective , 2008, Science.

[82]  P. Boyd,et al.  The biogeochemical cycle of iron in the ocean , 2010 .

[83]  Farooq Azam,et al.  Algicidal Bacteria in the Sea and their Impact on Algal Blooms1 , 2004, The Journal of eukaryotic microbiology.

[84]  C. Leboulanger,et al.  Diel variability of glycolate in the eastern tropical Atlantic Ocean , 1997 .

[85]  S. Pratt Quorum sensing by encounter rates in the ant Temnothorax albipennis , 2005 .

[86]  Kathryn M. Jones,et al.  How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model , 2007, Nature Reviews Microbiology.

[87]  D. Pesando,et al.  Investigations into a small fraction of volatile hydrocarbons , 1985 .

[88]  J. Crawford,et al.  Siderophores from neighboring organisms promote the growth of uncultured bacteria. , 2010, Chemistry & biology.

[89]  R. Feely,et al.  Ocean acidification: the other CO2 problem. , 2009, Annual review of marine science.

[90]  H. W. Reuszer MARINE BACTERIA AND THEIR RÔLE IN THE CYCLE OF LIFE IN THE SEA III. THE DISTRIBUTION OF BACTERIA IN THE OCEAN WATERS AND MUDS ABOUT CAPE COD , 1933 .

[91]  E. Shiner,et al.  Inter-kingdom signaling: deciphering the language of acyl homoserine lactones. , 2005, FEMS microbiology reviews.

[92]  R. Bohne,et al.  PHOSPHORUS CYCLING AND ALGAL-BACTERIAL COMPETITION IN SANDSFJORD, WESTERN NORWAY , 1993 .

[93]  Yann S. Dufour,et al.  H-NOX–mediated nitric oxide sensing modulates symbiotic colonization by Vibrio fischeri , 2010, Proceedings of the National Academy of Sciences.

[94]  D. J. Douglas,et al.  Enhancement of domoic acid production by reintroducing bacteria to axenic cultures of the diatom Pseudo-nitzschia multiseries. , 1995, Natural toxins.

[95]  J. Findlay,et al.  Antibacterial constituents of the diatom Navicula delognei. , 1984, Journal of natural products.

[96]  J. M. Meyer,et al.  Quorum-sensing and siderophore biosynthesis in Pseudomonas aeruginosa: lasR/lasI mutants exhibit reduced pyoverdine biosynthesis. , 1998, FEMS microbiology letters.

[97]  H. Ohtake,et al.  Involvement of an Extracellular Protease in Algicidal Activity of the Marine Bacterium Pseudoalteromonassp. Strain A28 , 2000, Applied and Environmental Microbiology.

[98]  James G. Mitchell,et al.  Marine bacterial organisation around point-like sources of amino acids. , 2003, FEMS microbiology ecology.

[99]  F. Azam,et al.  Cultivation and Ecosystem Role of a Marine Roseobacter Clade-Affiliated Cluster Bacterium , 2008, Applied and Environmental Microbiology.

[100]  D. Vaulot,et al.  IDENTIFICATION OF BACTERIA ASSOCIATED WITH DINOFLAGELLATES (DINOPHYCEAE) ALEXANDRIUM SPP. USING TYRAMIDE SIGNAL AMPLIFICATION–FLUORESCENT IN SITU HYBRIDIZATION AND CONFOCAL MICROSCOPY1 , 2002 .

[101]  D. Savage Microbial ecology of the gastrointestinal tract. , 1977, Annual review of microbiology.

[102]  V. Paul,et al.  Mini-review: quorum sensing in the marine environment and its relationship to biofouling , 2009, Biofouling.

[103]  P. Jonsson,et al.  Formation of harmful algal blooms cannot be explained by allelopathic interactions , 2009, Proceedings of the National Academy of Sciences.

[104]  S. Waksman,et al.  Relation of Bacteria to Diatoms In Sea Water , 1937, Journal of the Marine Biological Association of the United Kingdom.

[105]  L. Fauci,et al.  Nutrient transport and acquisition by diatom chains in a moving fluid , 2008, Journal of Fluid Mechanics.

[106]  C. Gobler,et al.  Most harmful algal bloom species are vitamin B1 and B12 auxotrophs , 2010, Proceedings of the National Academy of Sciences.

[107]  Jonathan J. Cole,et al.  INTERACTIONS BETWEEN BACTERIA AND ALGAE IN AQUATIC ECOSYSTEMS , 1982 .

[108]  A. Barreiro,et al.  Release and degradation of amnesic shellfish poison from decaying Pseudo-nitzschia multiseries in presence of bacteria and organic matter , 2007 .

[109]  Leszek Rychlewski,et al.  The Phaeodactylum genome reveals the evolutionary history of diatom genomes , 2008, Nature.

[110]  C. Carrano,et al.  Photolysis of iron–siderophore chelates promotes bacterial–algal mutualism , 2009, Proceedings of the National Academy of Sciences.

[111]  Adrian P. Martin,et al.  Persistence of cluster synchronization under the influence of advection. , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.

[112]  Liming Yan,et al.  Isolation and structural characterisation of two antibacterial free fatty acids from the marine diatom, Phaeodactylum tricornutum , 2008, Applied Microbiology and Biotechnology.

[113]  Michael R Droop Vitamins, Phytoplankton and Bacteria: Symbiosis or Scavenging? , 2007 .

[114]  K. Downing,et al.  Desulfovibrio magneticus RS-1 contains an iron- and phosphorus-rich organelle distinct from its bullet-shaped magnetosomes , 2010, Proceedings of the National Academy of Sciences.

[115]  M. T. Maldonado,et al.  The effect of Fe and Cu on growth and domoic acid production by Pseudo-nitzschia multiseries and Pseudo‐nitzschia australis , 2002 .

[116]  S. Gray,et al.  Symbiotic relations between bacteria and the domoic acid producing diatom Pseudo-nitzschia multiseries and the capacity of these bacteria for gluconic acid/gluconolactone formation , 1997 .

[117]  J. L. Martin,et al.  Links between Phytoplankton and Bacterial Community Dynamics in a Coastal Marine Environment , 2005, Microbial Ecology.

[118]  J. Gavis,et al.  Transport limitation of nutrient uptake in phytoplankton1 , 1974 .

[119]  M. Kodama,et al.  Direct contact between Pseudo-nitzschia multiseries and bacteria is necessary for the diatom to produce a high level of domoic acid , 2009, Fisheries Science.

[120]  G. Hardin The competitive exclusion principle. , 1960, Science.

[121]  F. Morel,et al.  SEQUENCE ANALYSIS AND TRANSCRIPTIONAL REGULATION OF IRON ACQUISITION GENES IN TWO MARINE DIATOMS 1 , 2007 .

[122]  K. Mann,et al.  Turbulence and the diffusive layers around small organisms , 1989 .

[123]  M. Merighi,et al.  Chlamydomonas reinhardtii Secretes Compounds That Mimic Bacterial Signals and Interfere with Quorum Sensing Regulation in Bacteria1 , 2004, Plant Physiology.

[124]  E. Ivanova,et al.  Phylogenetic relationships among marine Alteromonas-like proteobacteria: emended description of the family Alteromonadaceae and proposal of Pseudoalteromonadaceae fam. nov., Colwelliaceae fam. nov., Shewanellaceae fam. nov., Moritellaceae fam. nov., Ferrimonadaceae fam. nov., Idiomarinaceae fam. nov , 2004, International journal of systematic and evolutionary microbiology.

[125]  L. Hoffmann,et al.  Dynamic NanoSIMS ion imaging of unicellular freshwater algae exposed to copper , 2009, Analytical and bioanalytical chemistry.

[126]  Eunseog Youn,et al.  Human transcriptome analysis reveals a potential role for active transport in the metabolism of Pseudomonas aeruginosa autoinducers. , 2010, Microbes and infection.

[127]  F. Azam,et al.  Microbial structuring of marine ecosystems , 2007, Nature Reviews Microbiology.

[128]  R. Guillard,et al.  Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt, and Detonula confervacea (cleve) Gran. , 1962, Canadian journal of microbiology.

[129]  Kyung-Bum Lee,et al.  The hierarchical system of the 'Alphaproteobacteria': description of Hyphomonadaceae fam. nov., Xanthobacteraceae fam. nov. and Erythrobacteraceae fam. nov. , 2005, International journal of systematic and evolutionary microbiology.

[130]  G. E. Hutchinson,et al.  The Balance of Nature and Human Impact: The paradox of the plankton , 2013 .

[131]  Thomas Kiørboe,et al.  Abundance, size distribution and bacterial colonization of transparent exopolymeric particles (TEP) during spring in the Kattegat , 1996 .

[132]  M. Delledonne NO news is good news for plants. , 2005, Current opinion in plant biology.

[133]  A. Wichels,et al.  Species-Specific Bacterial Communities in the Phycosphere of Microalgae? , 2007, Microbial Ecology.

[134]  J. Chun,et al.  Taxonomic evaluation of the genera Ruegeria and Silicibacter: a proposal to transfer the genus Silicibacter Petursdottir and Kristjansson 1999 to the genus Ruegeria Uchino et al. 1999. , 2007, International journal of systematic and evolutionary microbiology.

[135]  D. Hogan Talking to Themselves: Autoregulation and Quorum Sensing in Fungi , 2006, Eukaryotic Cell.

[136]  D. Shih,et al.  Paraoxonase-2 deficiency enhances Pseudomonas aeruginosa quorum sensing in murine tracheal epithelia. , 2007, American journal of physiology. Lung cellular and molecular physiology.

[137]  K. Raymond,et al.  Petrobactin-mediated iron transport in pathogenic bacteria: coordination chemistry of an unusual 3,4-catecholate/citrate siderophore. , 2008, Journal of the American Chemical Society.

[138]  A. Allen,et al.  Copper‐dependent iron transport in coastal and oceanic diatoms , 2006 .

[139]  A. Wichels,et al.  Impacts of Cultivation of Marine Diatoms on the Associated Bacterial Community , 2007, Applied and Environmental Microbiology.

[140]  Hoon Kim,et al.  Gangjinia marincola gen. nov., sp. nov., a marine bacterium of the family Flavobacteriaceae. , 2011, International journal of systematic and evolutionary microbiology.

[141]  Ricardo Cavicchioli,et al.  Archaea — timeline of the third domain , 2011, Nature Reviews Microbiology.

[142]  K. Bruland,et al.  Domoic acid binds iron and copper: a possible role for the toxin produced by the marine diatom Pseudo-nitzschia , 2001 .

[143]  K. Schleifer,et al.  Phylogeny of the family Halomonadaceae based on 23S and 165 rDNA sequence analyses. , 2002, International journal of systematic and evolutionary microbiology.

[144]  A. Fernie,et al.  Evolution and metabolic significance of the urea cycle in photosynthetic diatoms , 2011, Nature.

[145]  J. Harder,et al.  Epiphytic bacteria on the Antarctic ice diatom Amphiprora kufferathii Manguin cleave hydrogen peroxide produced during algal photosynthesis. , 2008, Plant biology.

[146]  E. Delong,et al.  Archaeal dominance in the mesopelagic zone of the Pacific Ocean , 2001, Nature.

[147]  U. Passow Production of transparent exopolymer particles (TEP) by phyto- and bacterioplankton , 2002 .

[148]  P. Qian,et al.  Presence of Acyl-Homoserine Lactone in Subtidal Biofilm and the Implication in Larval Behavioral Response in the Polychaete Hydroides elegans , 2007, Microbial Ecology.

[149]  Alison Butler,et al.  Mechanistic considerations of halogenating enzymes , 2009, Nature.

[150]  Structure of the GAF domain, a ubiquitous signaling motif and a new class of cyclic GMP receptor , 2000, The EMBO journal.

[151]  R. Pistocchi,et al.  Bacterial-algal interactions in polysaccharide production , 1998 .

[152]  G. Caetano-Anollés,et al.  Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[153]  B. Bassler,et al.  Bacterial quorum-sensing network architectures. , 2009, Annual review of genetics.

[154]  D. Asker,et al.  Zeaxanthinibacter enoshimensis gen. nov., sp. nov., a novel zeaxanthin-producing marine bacterium of the family Flavobacteriaceae, isolated from seawater off Enoshima Island, Japan. , 2007, International journal of systematic and evolutionary microbiology.

[155]  E. K. Pikitch,et al.  Trophic Downgrading of Planet Earth , 2011, Science.

[156]  R. Rosen,et al.  GABA controls the level of quorum-sensing signal in Agrobacterium tumefaciens. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[157]  S. Shinoda,et al.  Structure and iron transport activity of vibrioferrin, a new siderophore of Vibrio parahaemolyticus. , 1994, Journal of biochemistry.

[158]  Vanessa Sperandio,et al.  Inter-kingdom signalling: communication between bacteria and their hosts , 2008, Nature Reviews Microbiology.

[159]  P. Dawyndt,et al.  Larkinella insperata gen. nov., sp. nov., a bacterium of the phylum 'Bacteroidetes' isolated from water of a steam generator. , 2006, International Journal of Systematic and Evolutionary Microbiology.

[160]  H. Rui,et al.  LuxO controls extracellular protease, haemolytic activities and siderophore production in fish pathogen Vibrio alginolyticus , 2007, Journal of applied microbiology.

[161]  Thomas Wichard,et al.  Lipid and Fatty Acid Composition of Diatoms Revisited: Rapid Wound‐Activated Change of Food Quality Parameters Influences Herbivorous Copepod Reproductive Success , 2007, Chembiochem : a European journal of chemical biology.

[162]  S. Sañudo-Wilhelmy,et al.  A new method for the determination of Vitamin B12 in seawater , 2004 .

[163]  A. Mearns-Spragg,et al.  A Fatty Acid from the Diatom Phaeodactylum tricornutum is Antibacterial Against Diverse Bacteria Including Multi-resistant Staphylococcus aureus (MRSA) , 2008, Marine Biotechnology.

[164]  S. Sañudo-Wilhelmy,et al.  Direct determination of vitamin B1 in seawater by solid‐phase extraction and high‐performance liquid chromatography quantification , 2005 .

[165]  W. Boland,et al.  Biosynthesis of the algal pheromone fucoserratene by the freshwater diatom Asterionella formosa (Bacillariophyceae) , 1998 .

[166]  G. Underwood,et al.  Diatom-Derived Carbohydrates as Factors Affecting Bacterial Community Composition in Estuarine Sediments , 2007, Applied and Environmental Microbiology.

[167]  Brian M. Hopkinson,et al.  Effect of Ocean Acidification on Iron Availability to Marine Phytoplankton , 2010, Science.

[168]  G. Muyzer,et al.  Genetic diversity of 'satellite' bacteria present in cultures of marine diatoms. , 2002, FEMS microbiology ecology.

[169]  R. Guillard,et al.  STUDIES OF MARINE PLANKTONIC DIATOMS:II. USE OF CYCLOTELLA NANA HUSTEDT FOR ASSAYS OF VITAMIN B12 IN SEA WATER , 1962 .

[170]  David A. Siegel,et al.  Climate-driven trends in contemporary ocean productivity , 2006, Nature.

[171]  G. Pohnert,et al.  The oxylipin chemistry of attraction and defense in brown algae and diatoms. , 2002, Natural product reports.

[172]  H. Grossart,et al.  Marine diatom species harbour distinct bacterial communities. , 2005, Environmental microbiology.

[173]  B. Jørgensen,et al.  Diffusive boundary layers of the colony‐forming plankton alga Phaeocystis sp.— implications for nutrient uptake and cellular growth , 1999 .

[174]  L. Richardson,et al.  Phytoplankton cell size and the development of microenvironments , 1995 .

[175]  H. Berg,et al.  Chemotaxis in Escherichia coli analysed by Three-dimensional Tracking , 1972, Nature.

[176]  A. Rosell‐Melé,et al.  Crenarchaea and phytoplankton coupling in sedimentary archives: Common trigger or metabolic dependence? , 2011 .

[177]  T. N. R. Srinivas,et al.  Rhodovulum imhoffii sp. nov. , 2007, International journal of systematic and evolutionary microbiology.

[178]  B. Jørgensen Bacteria and Marine Biogeochemistry , 2006 .

[179]  H. Ohta,et al.  Limnobacter litoralis sp. nov., a thiosulfate-oxidizing, heterotrophic bacterium isolated from a volcanic deposit, and emended description of the genus Limnobacter. , 2011, International journal of systematic and evolutionary microbiology.

[180]  M. Hay,et al.  Chemical cues induce consumer-specific defenses in a bloom-forming marine phytoplankton , 2007, Proceedings of the National Academy of Sciences.

[181]  M. R. Droop,et al.  Vitamin B12 and marine ecology , 1970, Helgoländer wissenschaftliche Meeresuntersuchungen.

[182]  Yuichi Kotani,et al.  Production of transparent exopolymer particles by four diatom species , 2010, Fisheries Science.

[183]  A. Butler,et al.  Photochemical cycling of iron in the surface ocean mediated by microbial iron(iii)-binding ligands , 2001, Nature.

[184]  G. Pohnert,et al.  Interactions of the Algicidal Bacterium Kordia algicida with Diatoms: Regulated Protease Excretion for Specific Algal Lysis , 2011, PloS one.

[185]  D. Gage Infection and Invasion of Roots by Symbiotic, Nitrogen-Fixing Rhizobia during Nodulation of Temperate Legumes , 2004, Microbiology and Molecular Biology Reviews.

[186]  S. Kjelleberg,et al.  Eukaryotic interference with homoserine lactone-mediated prokaryotic signalling , 1996, Journal of bacteriology.

[187]  H. Grossart,et al.  Direct observation of phytoplankton, TEP and aggregates on polycarbonate filters using brightfield microscopy , 1994 .

[188]  I. Furusawa,et al.  Characterization of cytoplasmic fibril structures found in gliding cells of Saprospira sp. , 2005, Canadian journal of microbiology.

[189]  M. Gelfand,et al.  Comparative Genomics of the Vitamin B12 Metabolism and Regulation in Prokaryotes* , 2003, Journal of Biological Chemistry.

[190]  C. Carrano,et al.  Boron binding by a siderophore isolated from marine bacteria associated with the toxic dinoflagellate Gymnodinium catenatum. , 2007, Journal of the American Chemical Society.

[191]  D. Stahl,et al.  Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria , 2009, Nature.

[192]  J. Ehrman,et al.  Diversity and distribution of epibiotic bacteria on Pseudo-nitzschia multiseries (Bacillariophyceae) in culture, and comparison with those on diatoms in native seawater , 2005 .

[193]  D. Mann,et al.  Novel Sex Cells and Evidence for Sex Pheromones in Diatoms , 2011, PloS one.

[194]  R. Bazzo,et al.  Molecular Insights into Quorum Sensing in the Human Pathogen Pseudomonas aeruginosa from the Structure of the Virulence Regulator LasR Bound to Its Autoinducer* , 2007, Journal of Biological Chemistry.

[195]  R. Guillard,et al.  GROWTH OF VITAMIN B12‐REQUIRING MARINE DIATOMS IN MIXED LABORATORY CULTURES WITH VITAMIN B12‐PRODUCING MARINE BACTERIA 1 2 , 1974 .

[196]  G. Pohnert,et al.  Biosynthesis of the algal pheromone hormosirene by the freshwater diatom Gomphonema parvulum (Bacillariophyceae) , 1996 .