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Everything Is Everywhere: Physiological Responses of the Mediterranean Sea and Eastern Pacific Ocean Epiphyte Cobetia Sp. to Varying Nutrient Concentration

  • Environmental Microbiology
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Abstract

Bacteria are essential in the maintenance and sustainment of marine environments (e.g., benthic systems), playing a key role in marine food webs and nutrient cycling. These microorganisms can live associated as epiphytic or endophytic populations with superior organisms with valuable ecological functions, e.g., seagrasses. Here, we isolated, identified, sequenced, and exposed two strains of the same species (i.e., identified as Cobetia sp.) from two different marine environments to different nutrient regimes using batch cultures: (1) Cobetia sp. UIB 001 from the endemic Mediterranean seagrass Posidonia oceanica and (2) Cobetia sp. 4B UA from the endemic Humboldt Current System (HCS) seagrass Heterozostera chilensis. From our physiological studies, both strains behaved as bacteria capable to cope with different nutrient and pH regimes, i.e., N, P, and Fe combined with different pH levels, both in long-term (12 days (d)) and short-term studies (4 d/96 h (h)). We showed that the isolated strains were sensitive to the N source (inorganic and organic) at low and high concentrations and low pH levels. Low availability of phosphorus (P) and Fe had a negative independent effect on growth, especially in the long-term studies. The strain UIB 001 showed a better adaptation to low nutrient concentrations, being a potential N2-fixer, reaching higher growth rates (μ) than the HCS strain. P-acquisition mechanisms were deeply investigated at the enzymatic (i.e., alkaline phosphatase activity, APA) and structural level (e.g., alkaline phosphatase D, PhoD). Finally, these results were complemented with the study of biochemical markers, i.e., reactive oxygen species (ROS). In short, we present how ecological niches (i.e., MS and HCS) might determine, select, and modify the genomic and phenotypic features of the same bacterial species (i.e., Cobetia spp.) found in different marine environments, pointing to a direct correlation between adaptability and oligotrophy of seawater.

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Data and Availability and Code Availability

This manuscript contains previously unpublished data. The name of the repository and accession number(s) are CP058244 to CP058245 (Cobetia sp. UIB 001) and CP059843 to CP059845 (Cobetia sp. 4B UA).

References

  1. Hemminga MA, Duarte CM (2002) Seagrass ecology. Cambridge University Press. James W. Fourqurean. https://doi.org/10.4319/lo.2002.47.2.0611

  2. Gutiérrez JL, Jones CG, Byers JE, Arkema KK, Berkenbusch K, Commito A et al (2012) Physical ecosystem engineers and the functioning of estuaries and coasts. Treatise Estuar Coast Sci 7:58–81. https://doi.org/10.1016/B978-0-12-374711-2.00705-1

    Article  Google Scholar 

  3. Renn CE (1937) Bacteria and the phosphorus cycle in the sea. Biol Bull 72:190–195

    Article  CAS  Google Scholar 

  4. Tortell PD, Maldonado MT, Price NM (1996) The role of heterotrophic bacteria in iron-limited ocean ecosystems. Nature. 383:330–332. https://doi.org/10.1038/383330a0

    Article  CAS  Google Scholar 

  5. Anderson OR (2018) Evidence for coupling of the carbon and phosphorus biogeochemical cycles in freshwater microbial communities. Front Mar Sci 5:1–6. https://doi.org/10.3389/fmars.2018.00020

    Article  Google Scholar 

  6. Flombaum P, Gallegos JL, Gordillo RA, Rincon J, Zabala LL, Jiao N, Karl DM, Li WKW, Lomas MW, Veneziano D, Vera CS, Vrugt JA, Martiny AC (2013) Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus. Proc Natl Acad Sci 110:9824–9829. https://doi.org/10.1073/pnas.1307701110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Ugarelli K, Chakrabarti S, Laas P, Stingl U (2017) The seagrass holobiont and its microbiome. Microorganisms 5:81. https://doi.org/10.3390/microorganisms5040081

    Article  CAS  PubMed Central  Google Scholar 

  8. Sohm JA, Webb EA, Capone DG (2011) Emerging patterns of marine nitrogen fixation. Nat Rev Microbiol 9:499–508. https://doi.org/10.1038/nrmicro2594

    Article  CAS  PubMed  Google Scholar 

  9. Agawin NSR, Ferriol P, Cryer C, Alcon E, Busquets A, Sintes E, Vidal C, Moyà G (2016) Significant nitrogen fixation activity associated with the phyllosphere of Mediterranean seagrass Posidonia oceanica: first report. Mar Ecol Prog Ser 551:53–62. https://doi.org/10.3354/meps11755

    Article  CAS  Google Scholar 

  10. Agawin NSR, Ferriol P, Sintes E, Moyà G (2017) Temporal and spatial variability of in situ nitrogen fixation activities associated with the Mediterranean seagrass Posidonia oceanica meadows. Limnol Oceanogr 62:2575–2592. https://doi.org/10.1002/lno.10591

    Article  CAS  Google Scholar 

  11. Agawin NSR, Ferriol P, Sintes E (2019) Simultaneous measurements of nitrogen fixation activities associated with different plant tissues of the seagrass Posidonia oceanica. Mar Ecol Prog Ser 611:111–127. https://doi.org/10.3354/meps12854

    Article  CAS  Google Scholar 

  12. Perry CJ, Dennison WC (1999) Microbial nutrient cycling in seagrass sediment. J Aust Geol Geophys 17:227–231

    Google Scholar 

  13. Tanhua T, Hainbucher D, Schroeder K, Cardin V, Álvarez M, Civitarese G (2013) The Mediterranean Sea system: a review and an introduction to the special issue. Ocean Sci 9:789–803. https://doi.org/10.5194/os-9-789-2013

    Article  Google Scholar 

  14. Thingstad TF, Krom MD, Mantoura RFC, Flaten GA, Groom S, Herut B, Kress N, Law CS, Pasternak A, Pitta P, Psarra S, Rassoulzadegan F, Tanaka T, Tselepides A, Wassmann P, Woodward EM, Riser CW, Zodiatis G, Zohary T (2005) Nature of phosphorus limitation in the ultraoligotrophic eastern Mediterranean. Science (80- ) 309:1068–1071. https://doi.org/10.1126/science.1112632

    Article  CAS  Google Scholar 

  15. Ridame C, Le Moal M, Guieu C et al (2011) Nutrient control of N2 fixation in the oligotrophic Mediterranean Sea and the impact of Saharan dust events. Biogeosciences 8:2773–2783. https://doi.org/10.5194/bg-8-2773-2011

    Article  CAS  Google Scholar 

  16. Statham PJ, Hart V (2005) Dissolved iron in the Cretan Sea (eastern Mediterranean). Limnol Oceanogr 50:1142–1148. https://doi.org/10.4319/lo.2005.50.4.1142

    Article  CAS  Google Scholar 

  17. Moore JK, Doney SC, Glover DM, Fung IY (2001) Iron cycling and nutrient-limitation patterns in surface waters of the world ocean. Deep Res Part II Top Stud Oceanogr 49:463–507. https://doi.org/10.1016/S0967-0645(01)00109-6

    Article  Google Scholar 

  18. Thiel M, Macaya EC, Acuña E, Arntz WE, Bastias H, Brokordt K, Camus PA, Castilla JC, Castro LR, Cortés M, Dumont CP, Escribano R, Fernández M, Gajardo JA, Gaymer CF, Gomez I, González AE, González HE, Haye PA et al (2007) The Humboldt Current System of Northern and Central Chile oceanographic processes, ecological interactions and socioeconomic feedback. Oceanogr Mar Biol 195–344

  19. Montecino V, Lange CB (2009) The Humboldt Current System: ecosystem components and processes, fisheries, and sediment studies. Prog Oceanogr 83:65–79. https://doi.org/10.1016/j.pocean.2009.07.041

    Article  Google Scholar 

  20. Kuo J (2005) A revision of the genus Heterozostera (Zosteraceae). Aquat Bot 81:97–140. https://doi.org/10.1016/j.aquabot.2004.10.005

    Article  Google Scholar 

  21. Smith TM, York PH, Broitman BR, Thiel M, Hays GC, van Sebille E, Putman NF, Macreadie PI, Sherman CDH (2018) Rare long-distance dispersal of a marine angiosperm across the Pacific Ocean. Glob Ecol Biogeogr 27:487–496. https://doi.org/10.1111/geb.12713

    Article  Google Scholar 

  22. Santelices B (1980) Phytogeographic characterization of the temperate coast of Pacific South America. Phycologia. 19:1–12. https://doi.org/10.2216/i0031-8884-19-1-1.1

    Article  Google Scholar 

  23. Mahowald NM, Hamilton DS, Mackey KRM, Moore JK, Baker AR, Scanza RA, Zhang Y (2018) Aerosol trace metal leaching and impacts on marine microorganisms. Nat Commun 9:2614. https://doi.org/10.1038/s41467-018-04970-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Moore CM, Mills MM, Arrigo KR, Berman-Frank I, Bopp L, Boyd PW, Galbraith ED, Geider RJ, Guieu C, Jaccard SL, Jickells TD, la Roche J, Lenton TM, Mahowald NM, Marañón E, Marinov I, Moore JK, Nakatsuka T, Oschlies A, Saito MA, Thingstad TF, Tsuda A, Ulloa O (2013) Processes and patterns of oceanic nutrient limitation. Nat Geosci 6:701–710. https://doi.org/10.1038/ngeo1765

    Article  CAS  Google Scholar 

  25. Bristow LA, Mohr W, Ahmerkamp S, Kuypers MMM (2017) Nutrients that limit growth in the ocean. Curr Biol 27:R474–R478. https://doi.org/10.1016/j.cub.2017.03.030

    Article  CAS  PubMed  Google Scholar 

  26. Sebastian M, Ammerman JW (2011) Role of the phosphatase PhoX in the phosphorus metabolism of the marine bacterium Ruegeria pomeroyi DSS-3. Environ Microbiol Rep 3:535–542. https://doi.org/10.1111/j.1758-2229.2011.00253.x

    Article  CAS  PubMed  Google Scholar 

  27. Lesser MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68:253–278

    Article  CAS  PubMed  Google Scholar 

  28. Yang M, Zhao W, Xie X (2014) Effects of nitrogen, phosphorus, iron and silicon on growth of five species of marine benthic diatoms. Acta Ecol Sin 34:311–319. https://doi.org/10.1016/j.chnaes.2014.10.003

    Article  Google Scholar 

  29. Garcia NS, Fu F, Sedwick PN, Hutchins DA (2015) Iron deficiency increases growth and nitrogen-fixation rates of phosphorus-deficient marine cyanobacteria. ISME J 9:238–245. https://doi.org/10.1038/ismej.2014.104

    Article  CAS  PubMed  Google Scholar 

  30. Fernández-Juárez V, Bennasar-Figueras A, Tovar-Sanchez A, Agawin NSR (2019) The role of iron in the P-acquisition mechanisms of the unicellular N2-fixing cyanobacteria Halothece sp., found in association with the Mediterranean seagrass Posidonia oceanica. Front Microbiol 10. https://doi.org/10.3389/fmicb.2019.01903

  31. Fernández-Juárez V, Bennasar-Figueras A, Sureda-Gomila A, Ramis-Munar G, Agawin NSR (2020) Differential effects of varying concentrations of phosphorus, iron, and nitrogen in N2-fixing cyanobacteria. Front Microbiol 11. https://doi.org/10.3389/fmicb.2020.541558

  32. Browning TJ, Achterberg EP, Yong JC, Rapp I, Utermann C, Engel A, Moore CM (2017) Iron limitation of microbial phosphorus acquisition in the tropical North Atlantic. Nat Commun 8:1–7. https://doi.org/10.1038/ncomms15465

    Article  CAS  Google Scholar 

  33. Baas-Becking LGM (1934) Geobiologie of inleiding tot de milieukunde. W.P. Van Stockum & Zoon, The Hague, the Netherlands

    Google Scholar 

  34. Sanz-Sáez I, Salazar G, Sánchez P, Lara E, Royo-Llonch M, Sà EL, Lucena T, Pujalte MJ, Vaqué D, Duarte CM, Gasol JM, Pedrós-Alió C, Sánchez O, Acinas SG (2020) Diversity and distribution of marine heterotrophic bacteria from a large culture collection. BMC Microbiol 20:1–16. https://doi.org/10.1186/s12866-020-01884-7

    Article  CAS  Google Scholar 

  35. Arahal DR, Ventosa A (2006) The family Halomonadaceae. In: E S (ed) The Prokaryotes. Springer, New York, pp 811–835

  36. De La Haba RR, Arahal DR, Márquez MC, Ventosa A (2010) Phylogenetic relationships within the family Halomonadaceae based on comparative 23S and 16S rRNA gene sequence analysis. Int J Syst Evol Microbiol 60:737–748. https://doi.org/10.1099/ijs.0.013979-0

    Article  CAS  PubMed  Google Scholar 

  37. Romanenko LA, Tanaka N, Svetashev VI, Falsen E (2013) Description of Cobetia amphilecti sp. nov., Cobetia litoralis sp. nov. and Cobetia pacifica sp. nov., classification of Halomonas halodurans as a later heterotypic synonym of Cobetia marina and emended descriptions of the genus Cobetia and Cobetia marina. Int J Syst Evol Microbiol 63:288–297. https://doi.org/10.1099/ijs.0.036863-0

    Article  CAS  PubMed  Google Scholar 

  38. Kim MS, Roh SW, Bae JW (2010) Cobetia crustatorum sp. nov., a novel slightly halophilic bacterium isolated from traditional fermented seafood in Korea. Int J Syst Evol Microbiol 60:620–626. https://doi.org/10.1099/ijs.0.008847-0

    Article  CAS  PubMed  Google Scholar 

  39. Arahal DR, Castillo AM, Ludwig W, Schleifer KH, Ventosa A (2002) Proposal of Cobetia marina gen. nov., comb. nov., within the family Halomonadaceae, to include the species Halomonas marina. Syst Appl Microbiol 25:207–211. https://doi.org/10.1078/0723-2020-00113

    Article  PubMed  Google Scholar 

  40. Yumoto I, Hirota K, Iwata H, Akutsu M, Kusumoto K, Morita N, Ezura Y, Okuyama H, Matsuyama H (2004) Temperature and nutrient availability control growth rate and fatty acid composition of facultatively psychrophilic Cobetia marina strain L-2. Arch Microbiol 181:345–351. https://doi.org/10.1007/s00203-004-0662-8

    Article  CAS  PubMed  Google Scholar 

  41. Ivanova EP, Christen R, Sawabe T, Alexeeva YV, Lysenko AM, Chelomin VP, Mikhailov VV (2005) Presence of ecophysiologically diverse populations within Cobetia marina strains isolated from marine invertebrate, algae and the environments. Microbes Environ 20:200–207. https://doi.org/10.1264/jsme2.20.200

    Article  Google Scholar 

  42. Ibacache-Quiroga C, Ojeda J, Espinoza-Vergara G, Olivero P, Cuellar M, Dinamarca MA (2013) The hydrocarbon-degrading marine bacterium Cobetia sp. strain MM1IDA2H-1 produces a biosurfactant that interferes with quorum sensing of fish pathogens by signal hijacking. Microb Biotechnol 6:394–405. https://doi.org/10.1111/1751-7915.12016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Lv N, Pan L, Zhang J, Li Y, Zhang M (2019) A novel micro-organism for removing excess ammonia-N in seawater ponds and the effect of Cobetia amphilecti on the growth and immune parameters of Litopenaeus vannamei. J World Aquacult Soc 50:448–459. https://doi.org/10.1111/jwas.12561

    Article  CAS  Google Scholar 

  44. Fernández-juárez V, López-alforja X, Frank-comas A, Echeveste P (2021) “The good, the bad and the double-sword” effects of microplastics and their organic additives in marine bacteria. Front Microbiol 11:1–12. https://doi.org/10.3389/fmicb.2020.581118

    Article  Google Scholar 

  45. Salvà Serra F, Salvà-Serra F, Svensson-Stadler L, Busquets A, Jaén-Luchoro D, Karlsson R, R. B. Moore E, Gomila M (2018) A protocol for extraction and purification of high-quality and quantity bacterial DNA applicable for genome sequencing: a modified version of the Marmur procedure. Protoc Exch. https://doi.org/10.1038/protex.2018.084

  46. Wick RR, Judd LM, Gorrie CL, Holt KE (2017) Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 13:e1005595. https://doi.org/10.1371/journal.pcbi.1005595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Gurevich A, Saveliev V, Vyahhi N, Tesler G (2013) QUAST: quality assessment tool for genome assemblies. Bioinformatics. 29:1072–1075. https://doi.org/10.1093/bioinformatics/btt086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Tatusova T, Dicuccio M, Badretdin A et al (2016) NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 44:6614–6624. https://doi.org/10.1093/nar/gkw569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Haft DH, DiCuccio M, Badretdin A, Brover V, Chetvernin V, O’Neill K, Li W, Chitsaz F, Derbyshire MK, Gonzales NR, Gwadz M, Lu F, Marchler GH, Song JS, Thanki N, Yamashita RA, Zheng C, Thibaud-Nissen F, Geer LY, Marchler-Bauer A, Pruitt KD (2018) RefSeq: an update on prokaryotic genome annotation and curation. Nucleic Acids Res 46:D851–D860. https://doi.org/10.1093/nar/gkx1068

    Article  CAS  PubMed  Google Scholar 

  50. Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617. https://doi.org/10.1099/ijsem.0.001755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Richter M, Rosselló-Móra R, Oliver Glöckner F, Peplies J (2016) JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics. 32:929–931. https://doi.org/10.1093/bioinformatics/btv681

    Article  CAS  PubMed  Google Scholar 

  53. Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 14:60. https://doi.org/10.1186/1471-2105-14-60

    Article  PubMed  PubMed Central  Google Scholar 

  54. Jaén-Luchoro D, Gonzales-Siles L, Karlsson R, Svensson-Stadler L, Molin K, Cardew S, Jensie-Markopolous S, Ohlén M, Inganäs E, Skovbjerg S, Tindall BJ, Moore ERB (2020) Corynebacterium sanguinis sp. nov., a clinical and environmental associated corynebacterium. Syst Appl Microbiol 43:126039. https://doi.org/10.1016/j.syapm.2019.126039

    Article  CAS  PubMed  Google Scholar 

  55. Contreras-Moreira B, Vinuesa P (2013) GET_HOMOLOGUES, a versatile software package for scalable and robust microbial pangenome analysis. Appl Environ Microbiol 79:7696–7701. https://doi.org/10.1128/aem.02411-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Huerta-Cepas J, Szklarczyk D, Heller D, Hernández-Plaza A, Forslund SK, Cook H, Mende DR, Letunic I, Rattei T, Jensen LJ, von Mering C, Bork P (2018) eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res 47:309–314. https://doi.org/10.1093/nar/gky1085

    Article  CAS  Google Scholar 

  57. Hillebrand H, Dürselen CD, Kirschtel D, Pollingher U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424. https://doi.org/10.1046/j.1529-8817.1999.3520403.x

    Article  Google Scholar 

  58. Zhang Y (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9:40. https://doi.org/10.1186/1471-2105-9-40

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, Potter SC, Punta M, Qureshi M, Sangrador-Vegas A, Salazar GA, Tate J, Bateman A (2016) The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res 44:D279–D285. https://doi.org/10.1093/nar/gkv1344

    Article  CAS  PubMed  Google Scholar 

  60. Li Z, Natarajan P, Ye Y, Hrabe T, Godzik A (2014) POSA: a user-driven, interactive multiple protein structure alignment server. Nucleic Acids Res 42:W240–W245. https://doi.org/10.1093/nar/gku394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Noskova Y, Likhatskaya G, Terentieva N, Son O, Tekutyeva L, Balabanova L (2019) A novel alkaline phosphatase/phosphodiesterase, CamPhoD, from marine bacterium Cobetia amphilecti KMM 296. Mar Drugs 17:1–20. https://doi.org/10.3390/md17120657

    Article  CAS  Google Scholar 

  62. The UniProt Consortium (2014) UniProt: a hub for protein information. Nucleic Acids Res 43:D204–D212. https://doi.org/10.1093/nar/gku989

    Article  CAS  PubMed Central  Google Scholar 

  63. DeLano WL (2002) The PyMOL molecular graphics system. Schrödinger, LLC. Available online at: http://www.pymol.org

  64. Park M, Kim C, Yang J, Lee H, Shin W, Kim S, Sa T (2005) Isolation and characterization of diazotrophic growth promoting bacteria from rhizosphere of agricultural crops of Korea. Microbiol Res 160:127–133. https://doi.org/10.1016/j.micres.2004.10.003

    Article  CAS  PubMed  Google Scholar 

  65. Hellweger FL, Huang Y, Luo H (2018) Carbon limitation drives GC content evolution of a marine bacterium in an individual-based genome-scale model. ISME J 12:1180–1187. https://doi.org/10.1038/s41396-017-0023-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Balabanova LA, Golotin VA, Kovalchuk SN, Babii AV, Shevchenko LS, Son OM, Kosovsky GY, Rasskazov VA (2016) The genome of the marine bacterium Cobetia marina KMM 296 isolated from the mussel Crenomytilus grayanus (dunker, 1853). Russ J Mar Biol 42:106–109. https://doi.org/10.1134/S106307401601003X

    Article  CAS  Google Scholar 

  67. Balabanova L, Nedashkovskaya O, Podvolotskaya A, Slepchenko L, Golotin V, Belik A, Shevchenko L, Son O, Rasskazov V (2016) Data supporting functional diversity of the marine bacterium Cobetia amphilecti KMM 296. Data Br 8:726–732. https://doi.org/10.1016/j.dib.2016.06.034

    Article  Google Scholar 

  68. Kuznetsov SI, Dubinina GA, Lapteva NA (1979) Biology of oligotrophic bacteria. Annu Rev Microbiol 33:377–387. https://doi.org/10.1146/annurev.mi.33.100179.002113

    Article  CAS  PubMed  Google Scholar 

  69. Schut F, Prins RA, Gottschal JC (1997) Oligotrophy and pelagic marine bacteria: facts and fiction. Aquat Microb Ecol 12:177–202

    Article  Google Scholar 

  70. Dao MH (2013) Reassessment of the cell surface area limitation to nutrient uptake in phytoplankton. Mar Ecol Prog Ser 489:87–92. https://doi.org/10.3354/meps10434

    Article  Google Scholar 

  71. Cole J, Findlay S, Pace M (1988) Bacterial production in fresh and saltwater ecosystems: a cross-system overview. Mar Ecol Prog Ser 43:1–10. https://doi.org/10.3354/meps043001

    Article  Google Scholar 

  72. Biddanda B, Ogdahl M, Cotner J (2001) Dominance of bacterial metabolism in oligotrophic relative to eutrophic waters. Limnol Oceanogr 46:730–739. https://doi.org/10.4319/lo.2001.46.3.0730

    Article  Google Scholar 

  73. Radwan S, Mahmoud H, Khanafer M, al-Habib A, al-Hasan R (2010) Identities of epilithic hydrocarbon-utilizing diazotrophic bacteria from the Arabian gulf coasts, and their potential for oil bioremediation without nitrogen supplementation. Microb Ecol 60:354–363. https://doi.org/10.1007/s00248-010-9702-x

    Article  CAS  PubMed  Google Scholar 

  74. Al-Awadhi H, Al-Mailem D, Dashti N et al (2012) Indigenous hydrocarbon-utilizing bacterioflora in oil-polluted habitats in Kuwait, two decades after the greatest man-made oil spill. Arch Microbiol 194:689–705. https://doi.org/10.1007/s00203-012-0800-7

    Article  CAS  PubMed  Google Scholar 

  75. Zhang Y, Burris RH, Ludden PW, Roberts GP (1997) Regulation of nitrogen fixation in Azospirillum brasilense. FEMS Microbiol Lett 152:195–204. https://doi.org/10.1016/S0378-1097(97)00187-0

    Article  CAS  PubMed  Google Scholar 

  76. Argandoña M, Fernández-Carazo R, Llamas I et al (2005) The moderately halophilic bacterium Halomonas maura is a free-living diazotroph. FEMS Microbiol Lett 244:69–74. https://doi.org/10.1016/j.femsle.2005.01.019

    Article  CAS  PubMed  Google Scholar 

  77. Yoshida N, Inaba S, Takagi H (2014) Utilization of atmospheric ammonia by an extremely oligotrophic bacterium, Rhodococcus erythropolis N9T-4. J Biosci Bioeng 117:28–32. https://doi.org/10.1016/j.jbiosc.2013.06.005

    Article  CAS  PubMed  Google Scholar 

  78. Sañudo-Wilhelmy SA, Kustka AB, Gobler CJ, Hutchins DA, Yang M, Lwiza K, Burns J, Capone DG, Raven JA, Carpenter EJ (2001) Phosphorus limitation of nitrogen fixation by Trichodesmium in the central Atlantic Ocean. Nature 411:66–69

    Article  PubMed  Google Scholar 

  79. Mackey KRM, Mioni CE, Ryan JP, Paytan A (2012) Phosphorus cycling in the red tide incubator region of Monterey Bay in response to upwelling. Front Microbiol 3:1–14. https://doi.org/10.3389/fmicb.2012.00033

    Article  CAS  Google Scholar 

  80. Hoffman BM, Lukoyanov D, Yang Z-Y, Dean DR, Seefeldt LC (2014) Mechanism of nitrogen fixation by nitrogenase: the next stage. Chem Rev 114:4041–4062. https://doi.org/10.1021/cr400641x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Shi D, Xu Y, Hopkinson BM, Morel FMM (2010) Effect of ocean acidification on iron availability to marine phytoplankton. Science (80- ) 327:676–679. https://doi.org/10.1126/science.1183517

    Article  CAS  Google Scholar 

  82. Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Annu Rev Mar Sci 1:169–192. https://doi.org/10.1146/annurev.marine.010908.163834

    Article  Google Scholar 

  83. Kadam PC, Boone DR (1996) Influence of pH on ammonia accumulation and toxicity in halophilic, methylotrophic methanogens. Appl Environ Microbiol 62:4486–4492. https://doi.org/10.1128/aem.62.12.4486-4492.1996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Ge C, Chai Y, Wang H, Kan M (2017) Ocean acidification: one potential driver of phosphorus eutrophication. Mar Pollut Bull 115:149–153. https://doi.org/10.1016/j.marpolbul.2016.12.016

    Article  CAS  PubMed  Google Scholar 

  85. Yu Plisova E, Balabanova LA, Ivanova EP, Kozhemyako VB, Mikhailov VV, Agafonova EV, Rasskazov VA (2005) A highly active alkaline phosphatase from the marine bacterium Cobetia. Mar Biotechnol 7:173–178. https://doi.org/10.1007/s10126-004-3022-4

    Article  CAS  Google Scholar 

  86. Balabanova L, Golotin V, Kovalchuk S, Bulgakov A, Likhatskaya G, Son O, Rasskazov V (2014) A novel bifunctional hybrid with marine bacterium alkaline phosphatase and far eastern holothurian mannan-binding lectin activities. PLoS One 9:e112729. https://doi.org/10.1371/journal.pone.0112729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Weidberg N, Ospina-Alvarez A, Bonicelli J, Barahona M, Aiken CM, Broitman BR, Navarrete SA (2020) Spatial shifts in productivity of the coastal ocean over the past two decades induced by migration of the Pacific anticyclone and Bakun’s effect in the Humboldt upwelling ecosystem. Glob Planet Chang 193:103259. https://doi.org/10.1016/j.gloplacha.2020.103259

    Article  Google Scholar 

  88. Troncoso VA, Daneri G, Cuevas LA, Jacob B, Montero P (2003) Bacterial carbon flow in the Humboldt Current System off Chile. Mar Ecol Prog Ser 250:1–12. https://doi.org/10.3354/meps250001

    Article  CAS  Google Scholar 

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Acknowledgements

VFJ acknowledges the travel funds provided by the Santander Iberoamérica 2019–2020 fellowship. We are grateful to Prof. Mario Edding and Felipe Sáez of the Laboratorio de Botánica Marina at the Universidad Católica del Norte for providing us with leaves of H. chilensis.

Funding

NSRA was funded through the Ministerio de Economía, Industria y Competitividad-Agencia Estatal de Investigación and the European Regional Development Funds project (CTM2016-75457-P). PE acknowledges the financial support of the research grants Fondecyt Iniciación 11170837, FONDEQUIP EQM120137, and REDI170403.

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Authors and Affiliations

  1. Marine Ecology and Systematics (MarES), Department of Biology, University of the Balearic Islands, Palma, Spain

    Víctor Fernández-Juárez & Nona S. R. Agawin

  2. Department of Infectious Diseases, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden

    Daniel Jaén-Luchoro

  3. Culture Collection University of Gothenburg (CCUG), Sahlgrenska Academy of the University of Gothenburg, Gothenburg, Sweden

    Daniel Jaén-Luchoro

  4. Instituto de Ciencias Naturales Alexander von Humboldt, Universidad de Antofagasta, Antofagasta, Chile

    Jocelyn Brito-Echeverría & Pedro Echeveste

  5. Grup de Microbiologia, Department of Biology, University of the Balearic Islands, Palma, Spain

    Antoni Bennasar-Figueras

  6. Instituto Milenio de Oceanografía, Concepción, Chile

    Pedro Echeveste

Authors
  1. Víctor Fernández-Juárez
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  2. Daniel Jaén-Luchoro
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  3. Jocelyn Brito-Echeverría
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  4. Nona S. R. Agawin
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  5. Antoni Bennasar-Figueras
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  6. Pedro Echeveste
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Contributions

VFJ and PE designed the experiments. VFJ conducted all the laboratory experiments and isolated the UIB 001 strain. JBE isolated the Pacific 4B UA strain. DJL conducted the bioinformatic analyses. All the authors, VFJ, DJL, JBE, ABF, NSRA, and PE, led the writing of the paper.

Corresponding author

Correspondence to Víctor Fernández-Juárez.

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The authors declare no competing interests.

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Fernández-Juárez, V., Jaén-Luchoro, D., Brito-Echeverría, J. et al. Everything Is Everywhere: Physiological Responses of the Mediterranean Sea and Eastern Pacific Ocean Epiphyte Cobetia Sp. to Varying Nutrient Concentration. Microb Ecol 83, 296–313 (2022). https://doi.org/10.1007/s00248-021-01766-z

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