Unveiling interactions mediated by B vitamins between diatoms and their associated bacteria from cocultures.

B vitamins Chaetoeroces spp. Pseudo‐nitzshia spp. coculture experiments phytoplankton–bacteria interactions

Journal

Journal of phycology
ISSN: 1529-8817
Titre abrégé: J Phycol
Pays: United States
ID NLM: 9882935

Informations de publication

Date de publication:
16 Oct 2024
Historique:
revised: 13 08 2024
received: 10 04 2024
accepted: 14 09 2024
medline: 16 10 2024
pubmed: 16 10 2024
entrez: 16 10 2024
Statut: aheadofprint

Résumé

Unveiling the interactions among phytoplankton and bacteria at the level of species requires axenic isolates to experimentally demonstrate their mutual effects. In this study, we describe the interactions among the diatoms Pseudo-nitzschia granii and Chaetoceros tenuissimus and their associated bacterial species, isolated from surface water of a coastal upwelling system using coculture experiments. Microalgae growth was assessed in axenic monocultures or in coculture with each of their co-isolated bacteria in the presence or absence of B vitamins. Pseudo-nitzschia granii growth was limited by B-vitamin supply, except when cultured with the bacteria Jannaschia cystaugens, which seemed to provide adequate levels of B vitamins to the diatom. Chaetoceros tenuissimus growth was reduced in the absence of B vitamins. Moreover, the growth of C. tenuissimus was stimulated by Alteromonas sp. and Celeribacter baekdonensis during the exponential growth. These results show a diversity of specific interactions between the diatoms and co-isolated bacteria, ranging from allelopathy to commensalism. Understanding how interactions between phytoplankton and bacteria modulate the structure and function of marine microbial plankton communities will contribute to a greater knowledge of plankton ecology and improve our ability to predict nutrient fluxes in marine ecosystems or the formation of blooms in a context of global change.

Identifiants

pubmed: 39413213
doi: 10.1111/jpy.13515
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Spanish Ministry of Economy and Competitiveness
ID : CTM2017-83362-R
Organisme : Xunta de Galicia
ID : PID2019-110011RB-C33
Organisme : Xunta de Galicia
ID : ED481A-2019/290

Informations de copyright

© 2024 The Author(s). Journal of Phycology published by Wiley Periodicals LLC on behalf of Phycological Society of America.

Références

Amin, S. A., Hmelo, L. R., van Tol, H. M., Durham, B. P., Carlson, L. T., Heal, K. R., Morales, R. L., Berthiaume, C. T., Parker, M. S., Djunaedi, B., Ingalls, A. E., Parsek, M. R., Moran, M. A., & Armbrust, E. V. (2015). Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature, 522(7554), 98–101. https://doi.org/10.1038/nature14488
Amin, S. A., Parker, M. S., & Armbrust, E. V. (2012). Interactions between diatoms and bacteria. Microbiology and Molecular Biology Reviews, 76(3), 667–684. https://doi.org/10.1128/MMBR.00007‐12
Andersen, R. A. (2015). Algal culturing techniques. Elsevier Academic.
Armbrust, E. (2009). The life of diatoms in the world's oceans. Nature, 459, 185–192. https://doi.org/10.1038/nature08057
Azam, F., & Malfatti, F. (2007). Microbial structuring of marine ecosystems. Nature Reviews Microbiology, 5(10), 782–791. https://doi.org/10.1038/nrmicro1747
Bates, S. S., Hubbard, K. A., Lundholm, N., Montresor, M., & Leaw, C. P. (2018). Pseudo‐nitzschia, Nitzschia, and domoic acid: New research since 2011. Harmful Algae, 79, 3–43. https://doi.org/10.1016/j.hal.2018.06.001
Bell, W., & Mitchell, R. (1972). Chemotactic and growth responses of marine bacteria to algal extracellular products. The Biological Bulletin, 143(2), 265–277. https://doi.org/10.2307/1540052
Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B: Methodological, 57(1), 289–300. https://doi.org/10.1111/j.2517‐6161.1995.tb02031.x
Bittner, M. J., Bannon, C. C., Rowland, E., Sundh, J., Bertrand, E. M., Andersson, A. F., Paerl, R. W., & Riemann, L. (2024). New chemical and microbial perspectives on vitamin B1 and vitamer dynamics of a coastal system. ISME Communications, 4(1), ycad016. https://doi.org/10.1093/ismeco/ycad016
Booth, B. C., Larouche, P., Bélanger, S., Klein, B., Amiel, D., & Mei, Z. P. (2002). Dynamics of Chaetoceros socialis blooms in the north water. Deep Sea Research Part II: Topical Studies in Oceanography, 49(22–23), 5003–5025. https://doi.org/10.1016/S0967‐0645(02)00175‐3
Buchan, A., LeCleir, G. R., Gulvik, C. A., & González, J. M. (2014). Master recyclers: Features and functions of bacteria associated with phytoplankton blooms. Nature Reviews Microbiology, 12(10), 686–698. https://doi.org/10.1038/nrmicro3326
Cho, B. C., & Azam, F. (1990). Biogeochemical significance of bacterial biomass in the ocean's euphotic zone. Marine Ecology Progress Series. Oldendor, 63(2), 253–259.
Coale, T. H., Bertrand, E. M., Lampe, R. H., & Allen, A. E. (2022). Molecular mechanisms underlying micronutrient utilization in marine diatoms. In A. Falciatore & T. Mock (Eds.),The molecular life of diatoms (pp. 567–604). Springer. https://doi.org/10.1007/978‐3‐030‐92499‐7_20
Cohen, N. R., Gong, W., Moran, D. M., McIlvin, M. R., Saito, M. A., & Marchetti, A. (2018). Transcriptomic and proteomic responses of the oceanic diatom Pseudo‐nitzschia granii to iron limitation. Environmental Microbiology, 20(8), 3109–3126. https://doi.org/10.1111/1462‐2920.14386
Costas‐Selas, C., Martínez‐García, S., Delgadillo‐Nuño, E., Justel‐Díez, M., Fuentes‐Lema, A., Fernández, E., & Teira, E. (2024). Linking the impact of bacteria on phytoplankton growth with microbial community composition and co‐occurrence patterns. Marine Environmental Research, 193, 106262. https://doi.org/10.1016/j.marenvres.2023.106262
Costas‐Selas, C., Martínez‐García, S., Logares, R., Hernández‐Ruiz, M., & Teira, E. (2023). Role of bacterial community composition as a driver of the small‐sized phytoplankton community structure in a productive coastal system. Microbial Ecology, 86(2), 777–794. https://doi.org/10.1007/s00248‐022‐02125‐2
Croft, M. T., Lawrence, A. D., Raux‐Deery, E., Warren, M. J., & Smith, A. G. (2005). Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature, 438(7064), 90–93. https://doi.org/10.1038/nature04056
Croft, M. T., Warren, M. J., & Smith, A. G. (2006). Algae need their vitamins. Eukaryotic Cell, 5(8), 1175–1183. https://doi.org/10.1128/EC.00097‐06
Cruz, B. N., & Neuer, S. (2022). Particle‐associated bacteria differentially influence the aggregation of the marine diatom Minutocellus polymorphus. ISME Communications, 2(1), 73. https://doi.org/10.1038/s43705‐022‐00146‐z
Dowling, D. P., Croft, A. K., & Drennan, C. L. (2012). Radical use of Rossmann and TIM barrel architectures for controlling coenzyme B12 chemistry. Annual Review of Biophysics, 41, 403–427. https://doi.org/10.1146/annurev‐biophys‐050511‐102225
Durham, B. P., Sharma, S., Luo, H., Smith, C. B., Amin, S. A., Bender, S. J., Dearth, S. P., van Mooy, B. A. S., Campagna, S. R., Kujawinski, E. B., Armbrust, E. V., & Moran, M. A. (2015). Cryptic carbon and sulfur cycling between surface ocean plankton. Proceedings of the National Academy of Sciences, 112(2), 453–457. https://doi.org/10.1073/pnas.1413137112
Edgar, R. C. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics, 26(19), 2460–2461. https://doi.org/10.1093/bioinformatics/btq461
Ellis, K. A., Cohen, N. R., Moreno, C., & Marchetti, A. (2017). Cobalamin‐independent methionine synthase distribution and influence on vitamin B12 growth requirements in marine diatoms. Protist, 168(1), 32–47. https://doi.org/10.1016/j.protis.2016.10.007
Falkowski, P. G. (1994). The role of phytoplankton photosynthesis in global biogeochemical cycles. Photosynthesis Research, 39, 235–258. https://doi.org/10.1007/BF00014586
Falkowski, P. G. (2012). Ocean science: The power of plankton. Nature, 483, S17–S20. https://doi.org/10.1038/483S17a
Field, C. B., Behrenfeld, M. J., Randerson, J. T., & Falkowski, P. (1998). Primary production of the biosphere: Integrating terrestrial and oceanic components. Science, 281(5374), 237–240. https://doi.org/10.1126/science.281.5374.237
Figueiras, F. G., Labarta, U., & Reiriz, M. F. (2002). Coastal upwelling, primary production and mussel growth in the Rías Baixas of Galicia. Hydrobiologia, 484, 121–131. https://doi.org/10.1023/A:1021309222459
Fraga, F. (1981). Upwelling off the Galician coast, northwest Spain. In F. A. Richards (Ed.), Coastal upwelling (Vol. 1, pp. 176–182). American Geophysical Union.
Fuhrman, J. A., Cram, J. A., & Needham, D. M. (2015). Marine microbial community dynamics and their ecological interpretation. Nature Reviews Microbiology, 13(3), 133–146. https://doi.org/10.1038/nrmicro3417
Gasol, J. M., & Del Giorgio, P. A. (2000). Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities. Scientia Marina, 64(2), 197–224. https://doi.org/10.3989/scimar.2000.64n2197
Goers, L., Freemont, P., & Polizzi, K. M. (2014). Co‐culture systems and technologies: Taking synthetic biology to the next level. Journal of the Royal Society Interface, 11(96), 20140065. https://doi.org/10.1098/rsif.2014.0065
Grant, M. A., Kazamia, E., Cicuta, P., & Smith, A. G. (2014). Direct exchange of vitamin B12 is demonstrated by modelling the growth dynamics of algal–bacterial cocultures. The ISME Journal, 8(7), 1418–1427. https://doi.org/10.1038/ismej.2014.9
Gross, J., & Ligges, U. (2015). nortest: Tests for Normality. R package version 1.0‐4. https://CRAN.R‐project.org/package=nortest
Grossart, H. P., Levold, F., Allgaier, M., Simon, M., & Brinkhoff, T. (2005). Marine diatom species harbour distinct bacterial communities. Environmental Microbiology, 7(6), 860–873. https://doi.org/10.1111/j.1462‐2920.2005.00759.x
Guannel, M. L., Horner‐Devine, M. C., & Rocap, G. (2011). Bacterial community composition differs with species and toxigenicity of the diatom Pseudo‐nitzschia. Aquatic Microbial Ecology, 64(2), 117–133. https://doi.org/10.3354/ame01513
Guillard, R. R. L. (2005). Purification methods for microalgae. In R. E. Andersen (Ed.), Algal culturing techniques (pp. 117–132). Elsevier Academic.
Helliwell, K. E., Wheeler, G. L., Leptos, K. C., Goldstein, R. E., & Smith, A. G. (2011). Insights into the evolution of vitamin B12 auxotrophy from sequenced algal genomes. Molecular Biology and Evolution, 28(10), 2921–2933. https://doi.org/10.1093/molbev/msr124
Joglar, V., Álvarez‐Salgado, X. A., Gago‐Martinez, A., Leao, J. M., Pérez‐Martínez, C., Pontiller, B., Lundin, D., Pinhassi, J., Fernández, E., & Teira, E. (2021). Cobalamin and microbial plankton dynamics along a coastal to offshore transect in the eastern North Atlantic Ocean. Environmental Microbiology, 23(3), 1559–1583. https://doi.org/10.1111/1462‐2920.15367
Johnson, W. M., Alexander, H., Bier, R. L., Miller, D. R., Muscarella, M. E., Pitz, K. J., & Smith, H. (2020). Auxotrophic interactions: A stabilizing attribute of aquatic microbial communities? FEMS Microbiology Ecology, 96(11), fiaa115. https://doi.org/10.1093/femsec/fiaa115
Joint, I., Henriksen, P., Fonnes, G. A., Bourne, D., Thingstad, T. F., & Riemann, B. (2002). Competition for inorganic nutrients between phytoplankton and bacterioplankton in nutrient manipulated mesocosms. Aquatic Microbial Ecology, 29(2), 145–159.
Justel‐Díez, M., Delgadillo‐Nuño, E., Gutiérrez‐Barral, A., García‐Otero, P., Alonso‐Barciela, I., Pereira‐Villanueva, P., Álvarez‐Salgado, X. A., Velando, A., Teira, E., & Fernández, E. (2023). Inputs of seabird guano alter microbial growth, community composition and the phytoplankton–bacterial interactions in a coastal system. Environmental Microbiology, 25, 1155–1173. https://doi.org/10.1111/1462‐2920.16349
Labeeuw, L., Bramucci, A. R., & Case, R. J. (2017). Bioactive small molecules mediate microalgal‐bacterial interactions. In M. Kumar & P. Ralph (Eds.), Systems biology of marine ecosystems (pp. 279–300). Springer.
Logares, R. (2017). ramalok/amplicon_processing: Workflow for Analysing MiSeq Amplicons based on Uparse (v1.5). Zenodo. https://doi.org/10.5281/zenodo.259579
Logares, R., Audic, S., Bass, D., Bittner, L., Boutte, C., Christen, R., Claverie, J. M., Decelle, J., Dolan, J. R., Dunthorn, M., Edvardsen, B., Gobet, A., Kooistra, W. H. C. F., Mahé, F., Not, F., Ogata, H., Pawlowski, J., Pernice, M. C., Romac, S., … Massana, R. (2014). Patterns of rare and abundant marine microbial eukaryotes. Current Biology, 24(8), 813–821. https://doi.org/10.1016/j.cub.2014.02.050
Luo, H., & Moran, M. A. (2014). Evolutionary ecology of the marine Roseobacter clade. Microbiology and Molecular Biology Reviews, 78(4), 573–587. https://doi.org/10.1128/mmbr.00020‐14
Malviya, S., Scalco, E., Audic, S., Vincent, F., Veluchamy, A., Poulain, J., Wincker, P., Iudicone, D., de Vargas, C., Bittner, L., Zingone, A., & Bowler, C. (2016). Insights into global diatom distribution and diversity in the world's ocean. Proceedings of the National Academy of Sciences, 113(11), E1516–E1525. https://doi.org/10.1073/pnas.1509523113
Marie, D., Le Gall, F., Edern, R., Gourvil, P., & Vaulot, D. (2017). Improvement of phytoplankton culture isolation using single cell sorting by flow cytometry. Journal of Phycology, 53(2), 271–282. https://doi.org/10.1111/jpy.12495
Matthews, R. G., Smith, A. E., Zhou, Z. S., Taurog, R. E., Bandarian, V., Evans, J. C., & Ludwig, M. (2003). Cobalamin‐dependent and cobalamin‐independent methionine synthases: Are there two solutions to the same chemical problem? Helvetica Chimica Acta, 86(12), 3939–3954. https://doi.org/10.1002/hlca.200390329
Mayali, X., & Azam, F. (2004). Algicidal bacteria in the sea and their impact on algal blooms. Journal of Eukaryotic Microbiology, 51(2), 139–144. https://doi.org/10.1111/j.1550‐7408.2004.tb00538.x
Meyer, N., Bigalke, A., Kaulfuß, A., & Pohnert, G. (2017). Strategies and ecological roles of algicidal bacteria. FEMS Microbiology Reviews, 41(6), 880–899. https://doi.org/10.1093/femsre/fux029
Nelson, D. M., Treguer, P., Brzezinski, M. A., Leynaert, A., & Queguiner, B. (1995). Production and dissolution of biogenic silica in the ocean: Revised global estimates, comparison with regional data and relationship to biogenic sedimentation. Global Biogeochemical Cycles, 9(3), 359–372. https://doi.org/10.1029/95GB01070
Nikolenko, S. I., Korobeynikov, A. I., & Alekseyev, M. A. (2013). BayesHammer: Bayesian clustering for error correction in single‐cell sequencing. BMC Genomics, 14, S7. https://doi.org/10.1186/1471‐2164‐14‐S1‐S7
Parada, A. E., Needham, D. M., & Fuhrman, J. A. (2016). Every base matters: Assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environmental Microbiology, 18(5), 1403–1414. https://doi.org/10.1111/1462‐2920.13023
Paul, C., & Pohnert, G. (2011). Interactions of the algicidal bacterium Kordia algicida with diatoms: Regulated protease excretion for specific algal lysis. PLoS ONE, 6(6), e21032. https://doi.org/10.1371/journal.pone.0021032
Pohlert, T. (2014). The Pairwise Multiple Comparison of Mean Ranks Package (PMCMR). R package. http://CRAN.R‐project.org/package=PMCMR
Prieto, A., Barber‐Lluch, E., Hernández‐Ruiz, M., Martínez‐García, S., Fernández, E., & Teira, E. (2016). Assessing the role of phytoplankton–bacterioplankton coupling in the response of microbial plankton to nutrient additions. Journal of Plankton Research, 38(1), 55–63. https://doi.org/10.1093/plankt/fbv101
Provasoli, L. (1974). Vitamins and growth regulators. In W. D. P. Stewart (Ed.), Algal physiology and biochemistry (pp. 741–787). Blackwell Scientific.
Ramanan, R., Kim, B. H., Cho, D. H., Oh, H. M., & Kim, H. S. (2016). Algae–bacteria interactions: Evolution, ecology and emerging applications. Biotechnology Advances, 34(1), 14–29. https://doi.org/10.1016/j.biotechadv.2015.12.003
Read, B. A., Kegel, J., Klute, M. J., Kuo, A., Lefebvre, S. C., Maumus, F., Mayer, C., Miller, J., Monier, A., Salamov, A., Young, J., Aguilar, M., Claverie, J. M., Frickenhaus, S., Gonzalez, K., Herman, E. K., Lin, Y. C., Napier, J., Ogata, H., … Grigoriev, I. V. (2013). Pan genome of the phytoplankton Emiliania underpins its global distribution. Nature, 499(7457), 209–213. https://doi.org/10.1038/nature12221
Ribalet, F., Intertaglia, L., Lebaron, P., & Casotti, R. (2008). Differential effect of three polyunsaturated aldehydes on marine bacterial isolates. Aquatic Toxicology, 86(2), 249–255. https://doi.org/10.1016/j.aquatox.2007.11.005
Sañudo‐Wilhelmy, S. A., Gomez‐Consarnau, L., Suffridge, C., & Webb, E. A. (2014). The role of B vitamins in marine biogeochemistry. Annual Review of Marine Science, 6, 339–367. https://doi.org/10.1146/annurev‐marine‐120710‐100912
Schirmer, M., Ijaz, U. Z., D'Amore, R., Hall, N., Sloan, W. T., & Quince, C. (2015). Insight into biases and sequencing errors for amplicon sequencing with the Illumina MiSeq platform. Nucleic Acids Research, 43(6), e37. https://doi.org/10.1093/nar/gku1341
Schowen, R. (1998). Thiamine‐dependent enzymes. In M. Sinnott (Ed.), Comprehensive biological catalysis (pp. 217–266). Academic Press.
Seymour, J. R., Amin, S. A., Raina, J. B., & Stocker, R. (2017). Zooming in on the phycosphere: The ecological interface for phytoplankton–bacteria relationships. Nature Microbiology, 2(7), 17065. https://doi.org/10.1038/nmicrobiol.2017.65
Shibl, A. A., Isaac, A., Ochsenkühn, M. A., Cárdenas, A., Fei, C., Behringer, G., Arnoux, M., Drou, N., Santos, M. P., Gunsalus, K. C., Voolstra, C. R., & Amin, S. A. (2020). Diatom modulation of select bacteria through use of two unique secondary metabolites. Proceedings of the National Academy of Sciences, 117(44), 27445–27455. https://doi.org/10.1073/pnas.2012088117
Shishlyannikov, S. M., Zakharova, Y. R., Volokitina, N. A., Mikhailov, I. S., Petrova, D. P., & Likhoshway, Y. V. (2011). A procedure for establishing an axenic culture of the diatom Synedra acus subsp. radians (Kütz.) Skabibitsch. From Lake Baikal. Limnology and Oceanography: Methods, 9(10), 478–484. https://doi.org/10.4319/lom.2011.9.478
Sittmann, J., Bae, M., Mevers, E., Li, M., Quinn, A., Sriram, G., Clardy, J., & Liu, Z. (2021). Bacterial diketopiperazines stimulate diatom growth and lipid accumulation. Plant Physiology, 186(2), 1159–1170. https://doi.org/10.1093/plphys/kiab080
Stewart, J. E., Marks, L. J., Gilgan, M. W., Pfeiffer, E., & Zwicker, B. M. (1998). Microbial utilization of the neurotoxin domoic acid: Blue mussels (Mytilus edulis) and soft shell clams (Mya arenaria) as sources of the microorganisms. Canadian Journal of Microbiology, 44(5), 456–464.
Streit, W. R., & Entcheva, P. (2003). Biotin in microbes, the genes involved in its biosynthesis, its biochemical role and perspectives for biotechnological production. Applied Microbiology and Biotechnology, 61, 21–31. https://doi.org/10.1007/s00253‐002‐1186‐2
Sultana, S., Bruns, S., Wilkes, H., Simon, M., & Wienhausen, G. (2023). Vitamin B12 is not shared by all marine prototrophic bacteria with their environment. The ISME Journal, 17, 836–845. https://doi.org/10.1038/s41396‐023‐01391‐3
Tang, Y. Z., Koch, F., & Gobler, C. J. (2010). Most harmful algal bloom species are vitamin B1 and B12 auxotrophs. Proceedings of the National Academy of Sciences, 107(48), 20756–20761. https://doi.org/10.1073/pnas.1009566107
Taylor, G. T., & Sullivan, C. W. 2008. Vitamin B12 and cobalt cycling among diatoms and bacteria in Antarctic sea ice microbial communities. Limnology and Oceanography 53(5), 1862–1877. https://doi.org/10.4319/lo.2008.53.5.1862
Tilstone, G. H., Miguez, B. M., Figueiras, F. G., & Fermín, E. G. (2000). Diatom dynamics in a coastal ecosystem affected by upwelling: Coupling between species succession, circulation and biogeochemical processes. Marine Ecology Progress Series, 205, 23–41. https://doi.org/10.3354/meps205023
Trainer, V. L., Bates, S. S., Lundholm, N., Thessen, A. E., Cochlan, W. P., Adams, N. G., & Trick, C. G. (2012). Pseudo‐nitzschia physiological ecology, phylogeny, toxicity, monitoring and impacts on ecosystem health. Harmful Algae, 14, 271–300. https://doi.org/10.1016/j.hal.2011.10.025
Van Tol, H. M., Amin, S. A., & Armbrust, E. V. (2017). Ubiquitous marine bacterium inhibits diatom cell division. The ISME Journal, 11(1), 31–42. https://doi.org/10.1038/ismej.2016.112
Vancaester, E., Depuydt, T., Osuna‐Cruz, C. M., & Vandepoele, K. (2020). Comprehensive and functional analysis of horizontal gene transfer events in diatoms. Molecular Biology and Evolution, 37(11), 3243–3257. https://doi.org/10.1093/molbev/msaa182
Vu, C. H. T., Lee, H. G., Chang, Y. K., & Oh, H. M. (2018). Axenic cultures for microalgal biotechnology: Establishment, assessment, maintenance, and applications. Biotechnology Advances, 36(2), 380–396. https://doi.org/10.1016/j.biotechadv.2017.12.018
Wagner‐Döbler, I., Ballhausen, B., Berger, M., Brinkhoff, T., Buchholz, I., Bunk, B., Cypionka, H., Daniel, R., Drepper, T., Gerdts, G., Hahnke, S., Han, C., Jahn, D., Kalhoefer, D., Kiss, H., Klenk, H. P., Kyrpides, N., Liebl, W., Liesegang, H., … Simon, M. (2010). The complete genome sequence of the algal symbiont Dinoroseobacter shibae: A hitchhiker's guide to life in the sea. The ISME Journal, 4(1), 61–77. https://doi.org/10.1038/ismej.2009.94
Wienhausen, G., Dlugosch, L., Jarling, R., Wilkes, H., Giebel, H. A., & Simon, M. (2022). Availability of vitamin B12 and its lower ligand intermediate α‐ribazole impact prokaryotic and protist communities in oceanic systems. The ISME Journal, 16(8), 2002–2014. https://doi.org/10.1038/s41396‐022‐01250‐7
Wienhausen, G., Noriega‐Ortega, B. E., Niggemann, J., Dittmar, T., & Simon, M. (2017). The exometabolome of two model strains of the Roseobacter group: A marketplace of microbial metabolites. Frontiers in Microbiology, 8, 1985. https://doi.org/10.3389/fmicb.2017.01985
Wildiers, E. (1901). Nouvelle substance indispensable au developpement de la levure [A new substance indispensable for the development of yeast.]. Cellule, 18, 313–331.
Xia, X., Zheng, Q., Leung, S. K., Wang, Y., Lee, P. Y., Jing, H., Jiao, N., & Liu, H. (2021). Distinct metabolic strategies of the dominant heterotrophic bacterial groups associated with marine Synechococcus. Science of the Total Environment, 798, 149208. https://doi.org/10.1016/j.scitotenv.2021.149208
Zhang, J., Kobert, K., Flouri, T., & Stamatakis, A. (2014). PEAR: A fast and accurate Illumina paired‐end reAd mergeR. Bioinformatics, 30(5), 614–620. https://doi.org/10.1093/bioinformatics/btt593
Zheng, Q., Lu, J., Wang, Y., & Jiao, N. (2019). Genomic reconstructions and potential metabolic strategies of generalist and specialist heterotrophic bacteria associated with an estuary Synechococcus culture. FEMS Microbiology Ecology, 95(3), fiz017. https://doi.org/10.1093/femsec/fiz017

Auteurs

Cecilia Costas-Selas (C)

Departamento de Ecoloxía e Bioloxía Animal, Centro de Investigación Mariña, Universidade de Vigo, Vigo, Spain.

Sandra Martínez-García (S)

Departamento de Ecoloxía e Bioloxía Animal, Centro de Investigación Mariña, Universidade de Vigo, Vigo, Spain.

Jarone Pinhassi (J)

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

Emilio Fernández (E)

Departamento de Ecoloxía e Bioloxía Animal, Centro de Investigación Mariña, Universidade de Vigo, Vigo, Spain.

Eva Teira (E)

Departamento de Ecoloxía e Bioloxía Animal, Centro de Investigación Mariña, Universidade de Vigo, Vigo, Spain.

Classifications MeSH