Cobalamin and microbial plankton dynamics along a coastal to offshore transect in the Eastern North Atlantic Ocean.


Journal

Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692

Informations de publication

Date de publication:
03 2021
Historique:
revised: 17 12 2020
received: 17 03 2020
accepted: 17 12 2020
pubmed: 22 12 2020
medline: 16 10 2021
entrez: 21 12 2020
Statut: ppublish

Résumé

Cobalamin (B12) is an essential cofactor that is exclusively synthesized by some prokaryotes while many prokaryotes and eukaryotes require an external supply of B12. The spatial and temporal availability of B12 is poorly understood in marine ecosystems. Field measurements of B12 along with a large set of ancillary biotic and abiotic factors were obtained during three oceanographic cruises in the NW Iberian Peninsula, covering different spatial and temporal scales. B12 concentrations were remarkably low (<1.5 pM) in all samples, being significantly higher at the subsurface Eastern North Atlantic Central Water than at shallower depths, suggesting that B12 supply in this water mass is greater than demand. Multiple regression models excluded B12 concentration as predictive variable for phytoplankton biomass or production, regardless of the presence of B12-requiring algae. Prokaryote production was the best predictor for primary production, and eukaryote community composition was better correlated with prokaryote community composition than with nutritional resources, suggesting that biotic interactions play a significant role in regulating microbial communities. Interestingly, co-occurrence network analyses based on 16S and 18S rRNA sequences allowed the identification of significant associations between potential B12 producers and consumers (e.g. Thaumarchaeota and Dynophyceae, or Amylibacter and Ostreococcus respectively), which can now be investigated using model systems in the laboratory.

Identifiants

pubmed: 33346385
doi: 10.1111/1462-2920.15367
doi:

Substances chimiques

Vitamin B 12 P6YC3EG204

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1559-1583

Informations de copyright

© 2020 Society for Applied Microbiology and John Wiley & Sons Ltd.

Références

Álvarez-Salgado, X.A., Figueiras, F.G., Pérez, F.F., Groom, S., Nogueira, E., Borges, A.V., et al. (2003) The Portugal coastal counter current off NW Spain: new insights on its biogeochemical variability. Prog Oceanogr 56: 281-321.
Álvarez-Salgado, X.A., Gago, J., Míguez, B.M., Gilcoto, M., and Pérez, F.F. (2000) Surface waters of the NW Iberian margin: upwelling on the shelf versus outwelling of upwelled waters from the Rías Baixas. Estuar Coast Shelf Sci 51: 821-837.
Amin, S.A., Hmelo, L.R., Van Tol, H.M., Durham, B.P., Carlson, L.T., Heal, K.R., et al. (2015) Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 522: 98-101.
Amin, S.A., Parker, M.S., and Armbrust, E.V. (2012) Interactions between diatoms and bacteria. Microbiol Mol Biol Rev 76: 667-684.
Banerjee, R. (1997) The yin-Yang of cobalamin biochemistry. Chem Biol 4: 175-186.
Banerjee, R., and Ragsdale, S.W. (2003) The many faces of vitamin B 12: catalysis by Cobalamin-dependent enzymes. Annu Rev Biochem 72: 209-247.
Barber-Lluch, E., Hernández-Ruiz, M., Prieto, A., Fernández, E., and Teira, E. (2019) Role of vitamin B12 in the microbial plankton response to nutrient enrichment. Mar Ecol Prog Ser 626: 29-42.
Barton, E.D., Largier, J.L., Torres, R., Sheridan, M., Trasviña, A., Souza, A., et al. (2015) Coastal upwelling and downwelling forcing of circulation in a semi-enclosed bay: Ria de Vigo. Prog Oceanogr 134: 173-189.
Barton, E.D., Torres, R., Figueiras, F.G., Gilcoto, M., and Largier, J. (2016) Surface water subduction during a downwelling event in a semienclosed bay. J Geophys Res Ocean 121: 7088-7107.
Bertrand, E.M., and Allen, A.E. (2012) Influence of vitamin B auxotrophy on nitrogen metabolism in eukaryotic phytoplankton. Front Microbiol 3: 1-16.
Bertrand, E.M., Allen, A.E., Dupont, C.L., Norden-Krichmar, T.M., Bai, J., Valas, R.E., and Saito, M.A. (2012) Influence of cobalamin scarcity on diatom molecular physiology and identification of a cobalamin acquisition protein. Proc Natl Acad Sci 109: E1762-E1771.
Bertrand, E.M., McCrow, J.P., Moustafa, A., Zheng, H., McQuaid, J.B., Delmont, T.O., et al. (2015) Phytoplankton-bacterial interactions mediate micronutrient colimitation at the coastal Antarctic Sea ice edge. Proc Natl Acad Sci U S A 112: 9938-9943.
Bertrand, E.M., Moran, D.M., McIlvin, M.R., Hoffman, J.M., Allen, A.E., and Saito, M.A. (2013) Methionine synthase interreplacement in diatom cultures and communities: implications for the persistence of B12 use by eukaryotic phytoplankton. Limnol Oceanogr 58: 1431-1450.
Bertrand, E.M., Saito, M.A., Lee, P.A., Dunbar, R.B., Sedwick, P.N., and Ditullio, G.R. (2011) Iron limitation of a springtime bacterial and phytoplankton community in the Ross Sea: implications for vitamin B12 nutrition. Front Microbiol 2: 1-12.
Biebl, H., Allgaier, M., Tindall, B.J., Koblizek, M., Lünsdorf, H., Pukall, R., and Wagner-Döbler, I. (2005) Dinoroseobacter shibae gen. nov., sp. nov., a new aerobic phototrophic bacterium isolated from dinoflagellates. Int J Syst Evol Microbiol 55: 1089-1096.
Blanton, J.O., Atkinson, L.P., Fernandez de Castillejo, F., and Lavin Montero, A. (1984) Coastal upwelling off the Rias Bajas, Galicia, Northwest Spain I: hydrographic studies. Reun ConsIntExplorMer 183: 79-90.
Brown, K.L. (2005) Chemistry and enzymology of vitamin B12. Chem Rev 105: 2075-2149.
Callahan, B.J., McMurdie, P.J., Rosen, M.J., Han, A.W., Johnson, A.J.A., and Holmes, S.P. (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13: 581-583.
Calvo-Díaz, A., and Morán, X.A.G. (2006) Seasonal dynamics of picoplankton in shelf waters of the southern Bay of Biscay. Aquat Microb Ecol 42: 159-174.
Carlucci, A.F., and Bowes, P.M. (1970) Vitamin production and utilization by phytoplankton in mixed culture. J Phycol 6: 393-400.
Carlucci, A.F., and Cuhel, R.L. (1977) Vitamins in the south polar seas: distribution and significance of dissolved and particulate vitamin B12, thiamine and biotin in the southern Indian Ocean. In Adaptations within Marine Ecosystems, Llano, G. (ed), (pp. 115-128). Washington: Smithsonian Institution.
Carlucci, A.F., Silbernagel, S.B., and McNally, P.M. (1969) Influence of temeprature and solar radiation on persistence of vitamin B12, thiamine and biotin in seawater. J Phycol 5: 302-305.
Cermeño, P., Marañón, E., Pérez, V., Serret, P., Fernández, E., and Castro, C.G. (2006) Phytoplankton size structure and primary production in a highly dynamic coastal ecosystem (Ría de Vigo, NW-Spain): seasonal and short-time scale variability. Estuar Coast Shelf Sci 67: 251-266.
Cirri, E., and Pohnert, G. (2019) Algae−bacteria interactions that balance the planktonic microbiome. New Phytol 223: 100-106.
Cohen, N.R., Ellis, A., Burns, W.G., Lampe, R.H., Schuback, N., Johnson, Z., et al. (2017) Iron and vitamin interactions in marine diatom isolates and natural assemblages of the Northeast Pacific Ocean. Limnol Oceanogr 62: 2076-2096.
Cooper, M.B., Kazamia, E., Helliwell, K.E., Kudahl, U.J., Sayer, A., Wheeler, G.L., and Smith, A.G. (2019) Cross-exchange of B-vitamins underpins a mutualistic interaction between ostreococcus tauri and dinoroseobacter shibae. ISME J 13: 334-345.
Cooper, M.B., and Smith, A.G. (2015) Exploring mutualistic interactions between microalgae and bacteria in the omics age. Curr Opin Plant Biol 26: 147-153.
Croft, M.T., Lawrence, A.D., Raux-Deery, E., Warren, M.J., and Smith, A.G. (2005) Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438: 90-93.
Croft, M.T., Warren, M.J., and Smith, A.G. (2006) Algae need their vitamins. Eukaryot Cell 5: 1175-1183.
Doxey, A.C., Kurtz, D.A., Lynch, M.D.J., Sauder, L.A., and Neufeld, J.D. (2015) Aquatic metagenomes implicate Thaumarchaeota in global cobalamin production. ISME J 9: 461-471.
Droop, M.R. (1957) Vitamin B12 in marine ecology. Nature 180: 1041-1042.
Dupont, C.L., Mccrow, J.P., Valas, R., Moustafa, A., Walworth, N., Goodenough, U., et al. (2015) Genomes and gene expression across light and productivity gradients in eastern subtropical Pacific microbial communities. ISME J 9: 1076-1092.
Durham, B.P., Sharma, S., Luo, H., Smith, C.B., Amin, S.A., Bender, S.J., et al. (2015) Cryptic carbon and sulfur cycling between surface ocean plankton. Proc Natl Acad Sci U S A 112: 453-457.
Elias, M., Gompert, Z., Jiggins, C., and Willmott, K. (2008) Mutualistic interactions drive ecological niche convergence in a diverse butterfly community. PLoS Biol 6: 2642-2649.
Ellis, K.A., Cohen, N.R., Moreno, C., and Marchetti, A. (2017) Cobalamin-independent methionine synthase distribution and influence on vitamin B12 growth requirements in marine diatoms. Protist 168: 32-47.
Elser, J.J., Stabler, L.B., and Hassett, R.P. (1995) Nutrient limitation of bacterial growth rates in lakes and oceans: a comparative study. Aquat Microb Ecol 9: 105-110.
Fernandes, A.D., Reid, J.N., Macklaim, J.M., McMurrough, T.A., Edgell, D.R., and Gloor, G.B. (2014) Unifying the analysis of high-throughput sequencing datasets: characterizing RNA-seq, 16S rRNA gene sequencing and selective growth experiments by compositional data analysis. Microbiome 2: 15.
Fernández-Castro, B., Mouriño-Carballido, B., Benítez-Barrios, V.M., Chouciño, P., Fraile-Nuez, E., Graña, R., et al. (2014) Microstructure turbulence and diffusivity parameterization in the tropical and subtropical Atlantic, Pacific and Indian oceans during the Malaspina 2010 expedition. Deep Res Part I Oceanogr Res Pap 94: 15-30.
Fietz, S., Martínez-Garcia, A., Rueda, G., Peck, V.L., Huguet, C., Escala, M., and Rosell-Melé, A. (2011) Crenarchaea and phytoplankton coupling in sedimentary archives: common trigger or metabolic dependence? Limnol Oceanogr 56: 1907-1916.
Figueiras, F.G., Abarta, U., and Fernández Reiriz, M.J. (2002) Coastal upwelling, primary production and mussel growth in the Rías Baixas of Galicia. Hydrobiologia 484: 121-131.
Fisher, T.R., Peele, E.R., Ammerman, J.W., and Jr, L.W.H. (1992) Nutrient limitation of phytoplankton in Chesapeake Bay. Mar Ecol Prog Ser 82: 51-63.
Fraga, F. (1981) Upwelling off the Galacian coast, Northwest Spain. In Coastal and Estuarine Sciences, Richards, F.A. (ed), (pp. 176-182). Washington: American Geophysical Union.
Gasol, J.M., and Del Giorgio, P.A. (2000) Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities. Sci Mar 64: 197-224.
Gloor, G.B., Macklaim, J.M., Pawlowsky-Glahn, V., and Egozcue, J.J. (2017) Microbiome datasets are compositional: and this is not optional. Front Microbiol 8: 1-6.
Gobler, C.J., Norman, C., Panzeca, C., Taylor, G.T., and Sañudo-Wilhelmy, S.A. (2007) Effect of B-vitamins (B1, B12) and inorganic nutrients on algal bloom dynamics in a coastal ecosystem. Aquat Microb Ecol 49: 181-194.
Gómez-Gesteira, M., de Castro, M., Prego, R., and Prez-Villar, V. (2001) An unusual two layered tidal circulation induced by stratification and wind in the Ría of Pontevedra (NW Spain). Estuar Coast Shelf Sci 52: 555-563.
Gong, W., Browne, J., Hall, N., Schruth, D., Paerl, H., and Marchetti, A. (2017) Molecular insights into a dinoflagellate bloom. ISME J 11: 439-452.
Gonzalez-Nuevo, G., Gago, J., and Cabanas, J.M. (2014) Upwelling index: a powerful tool for marine research in the NW Iberian upwelling system. J Oper Oceanogr 7: 47-57.
Grant, M.A., Kazamia, E., Cicuta, P., and Smith, A.G. (2014) Direct exchange of vitamin B12 is demonstrated by modelling the growth dynamics of algal-bacterial cocultures. ISME J 8: 1418-1427.
Grasshoff, K., Kremling, K., and Ehrhardt, M. (1999). Methods of Seawater Analysis. 3rd ed. Weinheim, Germany: Verlag Chemie.
Griffith, D.M., Veech, J.A., and Marsh, C.J. (2016) Cooccur: probabilistic species co-occurrence analysis in R. J Stat Softw 69: 1-17.
Guillou, L., Bachar, D., Audic, S., Bass, D., Berney, C., Bittner, L., et al. (2013) The Protist ribosomal reference database (PR2): a catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy. Nucleic Acids Res 41: D597-D604.
Haines, K.C., and Guillard, R.R.L. (1974) Growth of vitamin B12-requiring marine diatoms in mixed laboratory cultures with vitamin B12-producing marine bacteria. J Phycol 10: 245-252.
Heal, K.R., Carlson, L.T.R., Devol, A.H., Armbrust, E.V., Moffett, J.W., Stahl, D.A., and Ingalls, A.E. (2014) Determination of four forms of vitamin B12 and other B vitamins in seawater by liquid chromatography/tandem mass spectrometry. Rapid Commun Mass Spectrom 28: 2398-2404.
Heal, K.R., Qin, W., Ribalet, F., Bertagnolli, A.D., Coyote-Maestas, W., Hmelo, L.R., et al. (2017) Two distinct pools of B12 analogs reveal community interdependencies in the ocean. Proc Natl Acad Sci U S A 114: 364-369.
Helliwell, K.E. (2017) The roles of B vitamins in phytoplankton nutrition: new perspectives and prospects. New Phytol 216: 62-68.
Helliwell, K.E., Lawrence, A.D., Holzer, A., Kudahl, U.J., Sasso, S., Kräutler, B., et al. (2016) Cyanobacteria and eukaryotic algae use different chemical variants of vitamin B12. Curr Biol 26: 999-1008.
Helliwell, K.E., Scaife, M.A., Sasso, S., Paula, A., Araujo, U., Purton, S., and Smith, A.G. (2014) Unraveling vitamin B12-responsive gene regulation in algae. Plant Physiol 165: 388-397.
Helliwell, K.E., Wheeler, G.L., Leptos, K.C., Goldstein, R.E., and Smith, A.G. (2011) Insights into the evolution of vitamin B 12 auxotrophy from sequenced algal genomes. Mol Biol Evol 28: 2921-2933.
Hernández-Ruiz, M., Barber-Lluch, E., Prieto, A., Álvarez-Salgado, X.A., Logares, R., and Teira, E. (2018) Seasonal succession of small planktonic eukaryotes inhabiting surface waters of a coastal upwelling system. Environ Microbiol 20: 2955-2973.
Joglar, V., Prieto, A., Barber-Lluch, E., Hernández-Ruiz, M., Fernández, E., and Teira, E. (2020) Spatial and temporal variability in the response of phytoplankton and prokaryotes to B-vitamin amendments in an upwelling system. Biogeosciences 17: 2807-2823.
Joint, I., Hendrikson, P., Fonnes, G.A., Bourne, D., Thingstad, T.F., and Rieman, B. (2002) Competition for inorganic nutrients between phytoplankton and bacterioplancton in nutriend manipulated mesocosms. Aquat Microb Ecol 29: 145-159.
Juzeniene, A., Baturaite, Z., Lagunova, Z., Grigalavicius, M., Porojnicu, A.C., Bruland, Ø.S., and Moan, J. (2015) Influence of multiple UV exposures on serum cobalamin and vitamin D levels in healthy females. Scand J Public Health 43: 324-330.
Juzeniene, A., and Nizauskaite, Z. (2013) Photodegradation of cobalamins in aqueous solutions and in human blood. J Photochem Photobiol B Biol 122: 7-14.
Karl, D.M. (2002) Nutrient dynamics in the deep blue sea. Trends Microbiol 10: 410-418.
Kazamia, E., Czesnick, H., Van Nguyen, T.T., Croft, M.T., Sherwood, E., Sasso, S., et al. (2012) Mutualistic interactions between vitamin B12-dependent algae and heterotrophic bacteria exhibit regulation. Environ Microbiol 14: 1466-1476.
Koch, F., Hattenrath-Lehmann, T.K., Goleski, J.A., Sañudo-Wilhelmy, S., Fisher, N.S., and Gobler, C.J. (2012) Vitamin B1 and B12 uptake and cycling by plankton communities in coastal ecosystems. Front Microbiol 3: 1-11.
Koch, F., Burson, A., Tang, Y.Z., Collier, J.L., Fisher, N.S., Sañudo-Wilhelmy, S., and Gobler, C.J. (2014). Alteration of plankton communities and biogeochemical cycles by harmful Cochlodinium polykrikoides (Dinophyceae) blooms. Harmful Algae, 33, 41-54.
Koch, F., Marcoval, M.A., Panzeca, C., Bruland, K.W., Sañudo-Wilhelmy, S.A., and Gobler, C.J. (2011) The effect of vitamin B12 on phytoplankton growth and community structure in the Gulf of Alaska. Limnol Oceanogr 56: 1023-1034.
Koutmos, M., Datta, S., Pattridge, K.A., Smith, J.L., and Matthews, R.G. (2009) Insights into the reactivation of cobalamin-dependent methionine synthase. Proc Natl Acad Sci U S A 106: 18527-18532.
Liu, M., and Tanhua, T. (2019) Distribution of water masses in the Atlantic Ocean based on GLODAPv2. Ocean Sci Discuss: 1-32.
Logares, R., Sunagawa, S., Salazar, G., Cornejo-Castillo, F.M., Ferrera, I., Sarmento, H., et al. (2014) Metagenomic 16S rDNA Illumina tags are a powerful alternative to amplicon sequencing to explore diversity and structure of microbial communities. Environ Microbiol 16: 2659-2671.
Lovdal, T., Eichner, C., Grossart, H.P., Carbonnel, V., Chou, L., Martin-Jezequel, V., and Thingstad, T.F. (2008) Competition for inorganic and organic forms of nitrogen and phosphorous between phytoplankton and bacteria during an Emiliania huxleyi spring bloom. Biogeosciences 5: 371-383.
Madigan, M.T., Martinko, J., and Parker, J. (2005) Brock Biology of Micro-Organisms, 11th ed. Boston: Pearson; Prentice Hall.
Marañón, E., Holligan, P., Barciela, R., González, N., Mouriño, B., Pazó, M., and Varela, M. (2001) Patterns of phytoplankton size structure and productivity in contrasting open-ocean environments. Mar Ecol Prog Ser 216: 43-56.
Marsh, E.N. (1999) Coenzyme B12 (cobalamin)-dependent enzymes. Essays Biochem 34: 139-154.
Martens, J.H., Barg, H., Warren, M., and Jahn, D. (2002) Microbial production of vitamin B12. Appl Microbiol Biotechnol 58: 275-285.
Martínez-García, S., Fernández, E., Calvo-Díaz, A., Marañón, E., Morán, X.A.G., and Teira, E. (2010) Response of heterotrophic and autotrophic microbial plankton to inorganic and organic inputs along a latitudinal transect in the Atlantic Ocean. Biogeosciences 7: 1701-1713.
Massana, R., Gobet, A., Audic, S., Bass, D., Bittner, L., Boutte, C., et al. (2015) Marine protist diversity in European coastal waters and sediments as revealed by high-throughput sequencing. Environ Microbiol 17: 4035-4049.
Matthews, R.G., Smith, A.E., Zhou, Z.S., Taurog, R.E., Bandarian, V., Evans, J.C., and Ludwig, M. (2003) Cobalamin-dependent and cobalamin-independent methionine synthases: are there two solutions to the same chemical problem? Helv Chim Acta 86: 3939-3954.
Menzel, D.W., and Spaeth, J.P. (1962) Occurrence of vitamin B12 in the Sargasso Sea. Limnol Oceanogr 7: 151-154.
Monteverde, D.R., Gómez-Consarnau, L., Suffridge, C., and Sañudo-Wilhelmy, S.A. (2017) Life's utilization of B vitamins on early Earth. Geobiology 15: 3-18.
Moustafa, A., Evans, A.N., Kulis, D.M., Hackett, J.D., Erdner, D.L., Anderson, D.M., and Bhattacharya, D. (2010) Transcriptome profiling of a toxic dinoflagellate reveals a gene-rich protist and a potential impact on gene expression due to bacterial presence. PLoS One 5: e9688.
Norland, S (1993). The relationship between biomass and volume of bacteria. In Handboook of methods in aquatic microbial ecology, Kemp, P.F., Sherr, B.F., Sherr, E.B. and Cole, J.J. (eds.), (pp. 303-307). Boca Raton, FL: Lewis Publishers.
Okbamichael, M., and Sañudo-Wilhelmy, S.A. (2004) A new method for the determination of vitamin B12 in seawater. Anal Chim Acta 517: 33-38.
Paerl, R.W., Bertrand, E.M., Allen, A.E., Palenik, B., and Azam, F. (2015) Vitamin B1 ecophysiology of marine picoeukaryotic algae: strain-specific differences and a new role for bacteria in vitamin cycling. Limnol Oceanogr 60: 215-228.
Paerl, R.W., Sundh, J., Tan, D., Svenningsen, S.L., Hylander, S., Pinhassi, J., et al. (2018) Prevalent reliance of bacterioplankton on exogenous vitamin B1 and precursor availability. Proc Natl Acad Sci U S A 115: E10447-E10456.
Palenik, B., Grimwood, J., Aerts, A., Rouzé, P., Salamov, A., Putnam, N., et al. (2007) The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation. Proc Natl Acad Sci U S A 104: 7705-7710.
Panzeca, C., Beck, A.J., Tovar-Sanchez, A., Segovia-Zavala, J., Taylor, G.T., Gobler, C.J., and Sañudo-Wilhelmy, S.A. (2009) Distributions of dissolved vitamin B12 and co in coastal and open-ocean environments. Estuar Coast Shelf Sci 85: 223-230.
Parada, A.E., Needham, D.M., and Fuhrman, J.A. (2016) Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol 18: 1403-1414.
Piedracoba, S., Álvarez-Salgado, X.A., Rosón, G., and Herrera, J.L. (2005) Short-timescale thermohaline variability and residual circulation in the central segment of the coastal upwelling system of the Ría de Vigo (Northwest Spain) during four contrasting periods. J Geophys Res C Ocean 110: 1-15.
Piehler, M.F., Twomey, L.J., Hall, N.S., and Paerl, H.W. (2004) Impacts of inorganic nutrient enrichment on phytoplankton community structure and function in Pamlico sound, NC, USA. Estuar Coast Shelf Sci 61: 197-209.
Pollard, R.T., and Pu, S. (1985) Structure and circulation of the upper Atlantic Ocean northeast of the Azores. Prog Oceanogr 14: 443-462.
Provasoli, L. (1963) Organic regulation of phytoplankton fertility. sea 2: 165-219.
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., et al. (2012) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41: D590-D596.
Ríos, A.F., Pérez, F.F., and Fraga, F. (1992) Water masses in the upper and middle North Atlantic Ocean east of the Azores. Deep Sea Res Part A Oceanogr Res Pap 39: 645-658.
Rodionov, D.A., Vitreschak, A.G., Mironov, A.A., and Gelfand, M.S. (2003) Comparative genomics of the vitamin B12 metabolism and regulation in prokaryotes. J Biol Chem 278: 41148-41159.
Roth, J., Lawrence, J., and Bobik, T. (1996) Cobalamin (coenzyme B12): synthesis and biological significance. Annu Rev Microbiol 50: 137-181.
Sañudo-Wilhelmy, S.A., Cutter, L.S., Durazo, R., Smail, E.A., Gómez-Consarnau, L., Webb, E.A., et al. (2012) Multiple B-vitamin depletion in large areas of the coastal areas. Proc Natl Acad Sci U S A 109: 14041-14045.
Sañudo-Wilhelmy, S.A., Gobler, C.J., Okbamichael, M., and Taylor, G.T. (2006) Regulation of phytoplankton dynamics by vitamin B12. Geophys Res Lett 33: 10-13.
Sañudo-Wilhelmy, S.A., Gómez-Consarnau, L., Suffridge, C., and Webb, E.A. (2014) The role of B vitamins in marine biogeochemistry. Annu Rev Mar Sci 6: 339-367.
Seymour, J.R., Amin, S.A., Raina, J.B., and Stocker, R. (2017) Zooming in on the phycosphere: the ecological interface for phytoplankton-bacteria relationships. Nat Microbiol 2: 17065.
Shannon, P., Markiel, A., Ozier, O., Baliga, N.S., Wang, J.T., Ramage, D., et al. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13: 2498-2504.
Smith, D.C., and Azam, F. (1992) A simple, economical method for measuring bacterial protein synthesis rates in seawater using 3H-leucine1. Mar Microb Food Webs 6: 107-114.
Stupperich, E., and Krautler, B. (1988) Pseudo vitamin B12 or 5-ydroxybenzimidazolyl-cobamide are the corrinoids found in methanogenic bacteria. Arch Microbiol 149: 268-271.
Suffridge, C., Cutter, L., and Sañudo-Wilhelmy, S.A. (2017) A new analytical method for direct measurement of particulate and dissolved B-vitamins and their congeners in seawater. Front Mar Sci 4: 1-11.
Suffridge, C.P., Gómez-Consarnau, L., Monteverde, D.R., Cutter, L., Arístegui, J., Alvarez-Salgado, X.A., et al. (2018) B vitamins and their congeners as potential drivers of microbial community composition in an oligotrophic marine ecosystem. J Geophys Res Biogeo 123: 2890-2907.
Swift, D.G. (1981) Vitamin levels in the Gulf of Maine and ecological significance of vitamin B12 there. J Mar Res 39: 375-403.
Swift, D.G. (1980) Vitamins and phytoplankton growth. In The Physiological Ecology of Phytoplankton, Morris, I. (ed.), (pp. 329-368). Oxford: Blackwell Scientific Publications.
Tang, Y., Koch, F., and Gobler, C.J. (2010) Most harmful algal bloom species are vitamin B1 and B12 auxotrophs. Proc Natl Acad Sci 107: 20756-20761.
Taylor, G.T., and Sullivan, C.W. (2008) Vitamin B12 and cobalt cycling among diatoms and bacteria in Antarctic Sea ice microbial communities. Limnol Oceanogr 53: 1862-1877.
Teira, E., Aranguren-Gassis, M., González, J., Martínez-García, S., Pérez, P., and Serret, P. (2009) Influence of allochthonous matter on microbial community structure and function in an upwelling system off the Northwest Iberian Peninsula. Aquat Microb Ecol 55: 81-93.
Vaid, F.H.M., Zahid, S., Faiyaz, A., Qadeer, K., Gul, W., Anwar, Z., and Ahmad, I. (2018) Photolysis of methylcobalamin in aqueous solution: a kinetic study. J Photochem Photobiol A Chem 362: 40-48.
Veech, J.A. (2013) A probabilistic model for analysing species co-occurrence. Glob Ecol Biogeogr 22: 252-260.
Villegas-Mendoza, J., Cajal-Medrano, R., and Maske, H. (2019) B12 production by marine microbial communities and Dinoroseobacter shibae continuous cultures under different growth and respiration rates. Aquat Microb Ecol 83: 251-262.
Wagner-Döbler, I., Ballhausen, B., Berger, M., Brinkhoff, T., Buchholz, I., Bunk, B., et al. (2010) The complete genome sequence of the algal symbiont Dinoroseobacter shibae: a hitchhiker's guide to life in the sea. ISME J 4: 61-77.
Warren, M.J., Raux, E., Schubert, H.L., and Escalante-Semerena, J.C. (2002) The biosynthesis of adenosylcobalamin (vitamin B12). Nat Prod Rep 19: 390-412.
Watanabe, F., Katsura, H., Takenaka, S., Fujita, T., Abe, K., Tamura, Y., et al. (1999) Pseudovitamin B12 is the predominant cobamide of an algal health food, spirulina tablets. J Agric Food Chem 47: 4736-4741.
Wooster, W.S., Bakun, A., and McLain, D.R. (1976) Seasonal upwelling cycle along the eastern boundary of the north Atlantic. J Mar Res 34: 131-141.

Auteurs

Vanessa Joglar (V)

Centro de Investigación Mariña da Universidade de Vigo (CIM-UVIGO), Spain.
Departamento Ecoloxía e Bioloxía Animal, Universidade de Vigo, Campus Lagoas-Marcosende, Vigo, 36310, Spain.

Xosé Antón Álvarez-Salgado (XA)

CSIC, Instituto de Investigacións Mariñas, Eduardo Cabello 6, Vigo, 36208, Spain.

Ana Gago-Martinez (A)

Food and Analytical Chemistry Department, Chemistry Faculty, Department of Analytical and Food Chemistry, University of Vigo, Vigo, Campus Universitario de Vigo, 36310, Spain.

Jose M Leao (JM)

Food and Analytical Chemistry Department, Chemistry Faculty, Department of Analytical and Food Chemistry, University of Vigo, Vigo, Campus Universitario de Vigo, 36310, Spain.

Clara Pérez-Martínez (C)

Centre for Ecology and Evolution in Microbial Model Systems - EEMiS, Linnaeus University, Kalmar, Stuvaregatan 4, 39231, Sweden.

Benjamin Pontiller (B)

Centre for Ecology and Evolution in Microbial Model Systems - EEMiS, Linnaeus University, Kalmar, Stuvaregatan 4, 39231, Sweden.

Daniel Lundin (D)

Centre for Ecology and Evolution in Microbial Model Systems - EEMiS, Linnaeus University, Kalmar, Stuvaregatan 4, 39231, Sweden.

Jarone Pinhassi (J)

Centre for Ecology and Evolution in Microbial Model Systems - EEMiS, Linnaeus University, Kalmar, Stuvaregatan 4, 39231, Sweden.

Emilio Fernández (E)

Centro de Investigación Mariña da Universidade de Vigo (CIM-UVIGO), Spain.
Departamento Ecoloxía e Bioloxía Animal, Universidade de Vigo, Campus Lagoas-Marcosende, Vigo, 36310, Spain.

Eva Teira (E)

Centro de Investigación Mariña da Universidade de Vigo (CIM-UVIGO), Spain.
Departamento Ecoloxía e Bioloxía Animal, Universidade de Vigo, Campus Lagoas-Marcosende, Vigo, 36310, Spain.

Articles similaires

Populus Soil Microbiology Soil Microbiota Fungi
Coal Metagenome Phylogeny Bacteria Genome, Bacterial
Lakes Salinity Archaea Bacteria Microbiota
Rhizosphere Glycine max Seeds Soybean Oil Soil Microbiology

Classifications MeSH