Microbial ecology of the South Atlantic Subtropical Gyre: a state-of-the-art review of an understudied ocean region
DOI:
https://doi.org/10.1590/2675-2824069.20026lrf%20Keywords:
Marine Microbes, Bacterial Production, Biogeochemical Cycles, Oligotrophic Oceans, Pelagic SystemAbstract
Understanding the dynamics of microbial plankton communities, their metabolic processes and taxonomic composition
in oligotrophic ocean basins has been one of the central tasks of contemporary marine microbial ecology and one
of the main challenges in a changing global ocean. However, despite its ecological importance, the South Atlantic
Subtropical Gyre (SASG) remains poorly understood in relation to marine microbes, which comprise the major drivers of
biogeochemical cycles and the largest carbon sink to the deep ocean. This review presents the state of the art of microbial
ecology in the SASG, including the adjacent oligotrophic region, the Southwest Atlantic Ocean (SWAO). We have also
addressed the theoretical and methodological trends in this field since 1970s, focusing on the main milestones that led to
the more-detailed current knowledge of the role of oligotrophic gyres in the global carbon cycle. Finally, we discussed the
general patterns of microbial community composition in the SASG, focusing on their potential responses to environmental
factors. In spite of increasing efforts to investigate this region, SASG is among the least known oceanic provinces, which
has hampered the debate over whether the oligotrophic ocean acts as a sink or source of CO2
into the atmosphere.
References
ALLEN, R., HOFFMANN, L. J., LAW, C. S. & SUMMERFIELD, T. C. 2020. Subtle bacterioplankton community responses to elevated CO2 and warming in the oligotrophic South Pacific gyre. Environmental Microbiology Reports, 12(4), 377-386.
ALVES JUNIOR, N., MEIRELLES, P. M., SANTOS, E. O., DUTILH, B., SILVA, G. G. Z., PARANHOS, R., REZENDE, C. E., LIDA, T., MOURA, R.L., KRÜGER, R. H., SAWABE, T. & THOMPSON, F. 2015. Microbial community diversity and physical-chemical features of the Southwestern Atlantic Ocean. Archives of Microbiology, 197(2), 165-179.
ANDRADE, L., GONZALEZ, A. M., REZENDE, C. E., SUZUKI, M., VALENTIN, J. L. & PARANHOS, R. 2007. Distribution of HNA and LNA bacterial groups in the Southwest Atlantic Ocean. Brazilian Journal of Microbiology, 38(2), 330-336.
ANDRADE, L., GONZALEZ, A. M., VALENTIN, J. L. & PARANHOS, R. 2004. Bacterial abundance and production in the southwest Atlantic Ocean. Hydrobiologia, 511(1-3), 103-111.
ARÍSTEGUI, J. & HARRISON, W. G. 2002. Decoupling of primary production and community respiration in the ocean: implications for regional carbon studies. Aquatic Microbial Ecology, 29(2), 199-209.
AZAM, F., FENCHEL, J. T., FIELD, J. G., GRAY, S., MEYER-REIL, L. A. & THINGSTAD, T. F. 1983. The ecological role of water-column microbes in the sea. Marine Ecology Progress Series, 10, 257-263.
AZAM, F. & MALFATTI, F. 2007. Microbial structuring of marine ecosystems. Nature Reviews Microbiology, 5(10), 782-791.
BERGO, N. M., SIGNORI, C. N., AMADO, A. M., BRANDINI, F. P. & PELLIZARI, V. H. 2017. The partitioning of carbon biomass among the pico- and nano-plankton community in the South Brazilian Bight during a strong summer intrusion of South Atlantic Central Water. Frontiers in Marine Science, 4, 238.
BILLER, S. J., BERUBE, P. M., DOOLEY, K., WILLIAMS, M., SATINSKY, B. M., KACKL T., HOGLE, S. L., COE, A., BERGAUER, K., BOUMAN, H. A., BROWING, T. J., CORTE, D., HASSLER, C., HULSTON, D., JACQUOT, J. E., MASS, E. W., REINTHALER, T., SINTES, E., YOKOKAWA, T. & CHISHOLM, S.W. 2018. Marine microbial metagenomes sampled across space and time. Scientific Data, 5(1), 1-7.
BRANDINI, F. P., NOGUEIRA JUNIOR, M., SIMIÃO, M., CODINA, J. C. U. & NOERNBERG, M. A. 2014. Deep chlorophyll maximum and plankton community response to oceanic bottom intrusions on the continental shelf in the South Brazilian Bight. Continental Shelf Research, 89, 61-75. Deep chlorophyll maximum and plankton community response to oceanic bottom intrusions on the continental shelf in the South Brazilian Bight. Continental Shelf Research, 89, 61-75.
BRIX, H., GRUBER, N., KARL, D. M. & BATES, N. R. 2006. On the relationships between primary, net community, and export production in subtropical gyres. Deep Sea Research Part II: Topical Studies in Oceanography, 53(5-7), 698-717.
BRUSONI, S. & GEUNA, A. 2003. An international comparison of sectoral knowledge bases: Persistence and integration in the pharmaceutical industry. Research Policy, 32(10), 1897-1912.
CAMPBELL, L., NOLLA, H. A. & VAULOT, D. 1994. The importance of Prochlorococcus to community structure in the central North Pacific Ocean. Limnology and Oceanography, 39(4), 954-961.
CASTRO, B. M., BRANDINI, F. P., PIRES-VANIN, A. M. S. & MIRANDA, L. B. 2006. Multidisciplinary oceanographic processes on the Western Atlantic continental shelf between 4° N and 34° S. In: ALLAN, R. R. & KENNETH B. (eds.). The Sea Cambridge: Harvard University Press, pp. 209-251.
CHISHOLM, S. W., OLSON R. J. & YENTSCH C. M. 1988. Flow cytometry in oceanography: Status and prospects. Eos, Transactions of the American Geophysical Union, 69, 562-572.
CHO, B. C. & AZAM, F. 1988. Major role of bacteria in biogeochemical fluxes in the oceans’ interior. Nature, 332, 441-443.
CHO, B. C. & AZAM, F. 1990. Biogeochemical significance of bacterial biomass in the ocean’s euphotic zone. Marine Ecology Progress Series, 63(2), 253-259.
COLE, J. J., FINDLAY, S. & PACE, M. L. 1988. Bacterial production in fresh and saltwater ecosystems: a cross-system overview. Marine Ecology Progress Series, 43(1), 1-10.
COUTINHO, F. H., VON MEIJENFELDT, F. A. B., WALTER, J. M., HARO-MORENO, J. M., LOPÉZ-PÉREZ, M., VAN VERK, M. C., THOMPSON, C. C., COSENZA, C. A. N., APPOLINARIO, C. L., PARANHOS, R., CABRAL, A., DUTILH, B. E. & THOMPSON, F. L. 2021. Ecogenomics and metabolic potential of the South Atlantic Ocean microbiome. Science of the Total Environment, 765, 142758.
DEL GIORGIO, P. A. & COLE, J. J. 1998. Bacterial growth efficiency in natural aquatic systems. Annual Review of Ecology and Systematics, 29, 503-541.
DEL GIORGIO, P. A., COLE, J. J. & CIMBLERIS, A. 1997. Respiration rates in bacteria exceed phytoplankton production in unproductive aquatic systems. Nature, 385(6612), 148-151.
DELONG, E. F. 1992. Archaea in coastal marine environments. Proceedings of the National Academy of Sciences of the U.S.A., 89(12), 5685-5689.
DELONG, E. F., PRESTON, C. M., MINCER, T., RICH, V., HALLAM, S. J., FRIGAARD, N. U. & CHISHOLM, S. W. 2006. Community genomics among stratified microbial assemblages in the ocean’s interior. Science, 311(5760), 496-503.
DENTENER, F., KINNE, S., BOND, T., BOUCHER, O., COFALA, J., GENEROSO, S., GINOUX, P., GONG, S., HOELZEMANN, J. J., ITO, A., MARELLI, L., PENNER, J. E., PUTAUD, J. P., SCHULZ, M., VAN DER WERF, G. R. & WILSON, J. 2006. Emissions of primary aerosol and precursor gases in the years 2000 and 1750 prescribed data-sets for AeroCom. Atmospheric Chemistry and Physics, 6(12), 4321-4344,
DUARTE, C. M. 2015. Seafaring in the 21st century: the Malaspina 2010 circumnavigation expedition. Limnology and Oceanography Bulletin, 24(1), 11-14.
DUARTE, C. M., LOSADA, I. J., HENDRIKS, I. E., MAZARRASA, I. & MARBÀ, N. 2013. The role of coastal plant communities for climate change mitigation and adaptation. Nature Climate Change, 3(11), 961-968.
DUCE, R. A., LAROCHE, J., ALTIERI, K., ARRIGO, K. R., BAKER, A. R., CAPONE, D. G., CORNELL, S., DENTENER, F., GALLOWAY, J., GANESHRAM, R. S., GEIDER, R. J., JICHKELLS, T., KUYPERS, M. M., LANGLOIS, R., LISS, P. S., LIU, S. M., MIDDELBURG, J. J., MOORE, C. M., NICKOVIC, S., OSCHLIES, A., PEDERSON, T., PROSPERO, J., SCHILITZER, R., SEITZINGER, S., SORENSEN, L. L., UEMATSU, M., ULLOA, O., VOSS, M., WARD, B. & ZAMORA, L. 2008. Impacts of atmospheric anthropogenic nitrogen on the open ocean. Science, 320(5878), 893-897.
DUCKLOW, H. W. & KIRCHMAN, D. L. 1983. Bacterial dynamics and distribution during a spring diatom bloom in the Hudson River plume, USA. Journal of Plankton Research, 5(3), 333-355.
EVANS, C., GÓMEZ-PEREIRA, P. R., MARTIN, A. P., SCANLAN, D. J. & ZUBKOV, M. V. 2015. Photoheterotrophy of bacterioplankton is ubiquitous in the surface oligotrophic ocean. Progress in Oceanography, 135, 139-145.
FALCÓN, L. I., NOGUEZ, A. M., ESPINOSA-ASUAR, L., EGUIARTE, L. E. & SOUZA, V. 2008. Evidence of biogeography in surface ocean bacterioplankton assemblages. Marine Genomics, 1(2), 55-61.
FALKOWSKI, P. G. 2012. Ocean science: the power of plankton. Nature, 483(7387), S17-S20.
FALKOWSKI, P. G., FENCHEL, T. & DELONG, E. F. 2008. The microbial engines that drive earth’s biogeochemical Cycles. Science, 320(5879), 1034-1039.
FOGG, G. E. 1995. Some comments on picoplankton and its importance in the pelagic ecosystem. Aquatic Microbial Ecology, 9(1), 33-39.
FRAME, J. D. 1977. Mainstream research in Latin America and the Caribbean. lnterciencia, 2(3), 143-148.
FUHRMAN, J. A. 1999. Marine viruses and their biogeochemical and ecological effects. Nature, 399(6736), 541-548.
FUHRMAN, J. A. & AZAM, F. 1980. Bacterioplankton secondary production estimates for coastal waters of British Columbia, Antarctica, and California. Applied and Environmental Microbiology, 39(6), 1085-1095.
FUHRMAN, J. A. & AZAM, F. 1982. Thymidine incorporation as a measure of heterotrophic bacterioplankton production in marine surface waters: evaluation and field results. Marine Biology, 66, 109-120.
FUHRMAN, J. A., EPPLEY, R. W., HAGSTROM, A. & AZAM, F. 1985. Diel variations in bacterioplankton, phytoplankton, and related parameters in the Southern California Bight. Marine Ecology Progress Series, 27, 9-20.
FUHRMAN, J. A., SLEETER, T. D., CARLSON, C. A. & PROCTOR, L. M. 1989. Dominance of bacterial biomass in the Sargasso Sea and its ecological implications. Marine Ecology Progress Series, 57, 207-217.
GARCÍA-MARTÍN, E. E., ARANGUREN-GASSIS, M., HARTMANN, M., ZUBKOV, M. V. & SERRET, P. 2017. Contribution of bacterial respiration to plankton respiration from 50°N to 44°S in the Atlantic Ocean. Progress in Oceanography, 158, 99-108.
GASOL, J. M. & KIRCHMAN, D. L. 2018. Microbial ecology of the oceans. 3rd ed. Hoboken: Wiley-Blackwell.
GASOL, J. M., PINHASSI, J., ALONSO-SÁEZ, L., DUCKLOW, H., HERNDL, G. J., KOBLÍZEK, M., LABRENZ, M., LU, H., MORÁN, X. A. G., REINTHALER, T. & SIMON, M. 2008. Towards a better understanding of microbial carbon flux in the sea. Aquatic Microbial Ecology, 53, 21-38.
GASOL, J. M., VÁZQUEZ-DOMÍNGUEZ, E., VAQUÉ, D., AGUSTÍ, S. & DUARTE, C. M. 2009. Bacterial activity and diffusive nutrient supply in the oligotrophic Central Atlantic Ocean. Aquatic Microbial Ecology, 7(1), 1-12.
GIOVANNONI, S. J. 2017. SAR11 bacteria: the most abundant plankton in the oceans. Annual Review of Marine Science, 9, 231-255.
GIST, N., SERRET, P., WOODWARD, E. M. S., CHAMBERLAIN, K. & ROBINSON, C. 2009. Seasonal and spatial variability in plankton production and respiration in the Subtropical Gyres of the Atlantic Ocean. Deep Sea Research Part II: Topical Studies in Oceanography, 56(15), 931-940.
GONZÁLEZ, N., ANADÓN, R. & MARAÑÓN, E. 2002. Large-scale variability of planktonic net community metabolism in the Atlantic Ocean: importance of temporal changes in oligotrophic subtropical waters. Marine Ecology Progress Series, 233, 21-30.
GROSSART, H. P., MASSANA, R., MCMAHON, K. D. & WALSH, D. A. 2020. Linking metagenomics to aquatic microbial ecology and biogeochemical cycles. Limnology and Oceanography, 65(Suppl 1), S2-S20.
HAMMER, Ø, HARPER, D. A. T. & RYAN, P. D. 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4(1), 1-9.
HILL, K. L., RINTOUL, S. R., RIDGWAY, K. R. & OKE, P. R. 2011. Decadal changes in the South Pacific western boundary current system revealed in observations and ocean state estimates. Journal of Geophysical Research: Oceans, 116(C1), C01009.
HOBBIE, J. E. & COLE, J. J. 1984. Response of a detrital food web to eutrophication. Bulletin of Marine Science, 35(3), 357-363.
HOBBIE, J. E., DALEY, R. J. & JASPER, S. 1977. Use of nuclepore filters for counting bacteria by fluorescence microscopy. Applied and Environmental Microbiology, 33(5), 1225-1228.
HOPPE, H. G., BREITHAUPT, P., WALTHER, K., KOPPE, R., BLECK, S., SOMMER, U. & JÜRGENS, K. 2008. Climate warming in winter affects the coupling between phytoplankton and bacteria during the spring bloom: a mesocosm study. Aquatic Microbial Ecology, 51(2), 105-115.
HOPPE, H. G., GOCKE, K., KOPPE, R. & BEGLER, C. 2002. Bacterial growth and primary production along a north-south transect of the Atlantic Ocean. Nature, 416(6877), 168-171.
HOPPE, H. G., GOCKE, K., KOPPE, R. & KRAUS, G. 2006. Changing bacterioplankton growth characteristics on a large spatial scale: oligotrophic versus mesotrophic ocean. Marine Ecology Progress Series, 323, 21-33.
HU, Z. Z., KUMAR, A., JHA, B., ZHU, J. & HUANG, B. 2017. Persistence and predictions of the remarkable warm anomaly in the northeastern Pacific Ocean during 2014-16. Journal of Climate, 30(2), 689-702.
HUETE-STAUFFER, T. M., ARANDIA-GOROSTIDI, N., ALONSO-SÁEZ, L. & MORÁN, X. A. G. 2016. Experimental warming decreases the average size and nucleic acid content of marine bacterial communities. Frontiers in Microbiology, 7, 730.
HUTCHINS, D. A. & FU, F. 2017. Microorganisms and ocean global change. Nature Microbiology, 2(6), 17058.
IPCC (Intergovernmental Panel on Climate Change). STOCKER, T. F., QIN, D., PLATTNER, G., TIGNOR, M., ALLEN, S. K., BOSCHUNG, J., NAUEL, A., XIA, Y., BEX, V. & MIDGLEY, P. M. (eds.). Climate change 2013: the physical science basis. Cambridge: Cambridge University Press, pp. 1535.
JIAO, N. & AZAM, F. 2011. Microbial carbon pump and its significance for carbon sequestration in the ocean. Microbial Carbon Pump in the Ocean, 10, 43-45.
JIAO, N., HERNDL, G. J., HANSELL, D. A., BENNER, R., KATTNER, G., WILHELM, S. W. & AZAM, F. 2010. Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nature Reviews Microbiology, 8(8), 593-599.
JIAO, N., ROBINSON, C., AZAM, F., THOMAS, H., BALTAR, F., DANG, H., HARDMAN-MOUNTFORD, N. J., JOHNSON, M., KIRCHMAN, D. L., KOCH, B. P., LEGENDRE, L., LI, C., LIU, J., LUO, T., LUO, Y. W., MITRA, A., ROMANOU, A., TANG, K., WANG, X., ZHANG, C. & ZHANG, R. 2014. Mechanisms of microbial carbon sequestration in the ocean-future research directions. Biogeosciences, 11(19), 5285-5306.
KARL, D. M. 2007. Microbial oceanography: paradigms, processes and promise. Nature Reviews Microbiology, 5(10), 759-769.
KIRCHMAN, D. L. & HOCH, M. P. 1988. Bacterial production in the Delaware Bay estuary estimated from thymidine and leucine incorporation rates. Marine Ecology Progress Series, 45(1), 169-178.
KIRCHMAN, D. L., K’NEES, E. & HODSON, R. 1985. Leucine incorporation and its potential as a measure of protein synthesis by bacteria in natural aquatic systems. Applied and Environmental Microbiology, 49(3), 599-607.
KIRCHMAN, D. L., KEIL, R. G. & WHEELER, P. A. 1989. The effect of amino acids on ammonium utilization and regeneration by heterotrophic bacteria in the subarctic Pacific. Deep Sea Research Part A. Oceanographic Research Papers, 36(11), 1763-1776.
KUMARI, L. 2006. Trends in synthetic organic chemistry research. Cross-country comparison of activity index. Scientometrics, 67(3), 467-476.
LARA, E., ARRIETA, J. M., GARCIA-ZARANDONA, I., BORAS, J. A., DUARTE, C. M., AGUSTÍ, S., WASSMAN, P. & VAQUÉ, D. 2013. Experimental evaluation of the warming effect on viral, bacterial and protistan communities in two contrasting Arctic systems. Aquatic Microbial Ecology, 70(1), 17-32.
LÊ, S., JOSSE, J. & HUSSON, F. 2008. FactoMineR: a package for multivariate analysis. Journal of Statistical Software, 25(1), 1-18.
LEGENDRE, L., RIVKIN, R. B., WEINBAUER, M. G., GUIDI, L. & UITZ, J. 2015. The microbial carbon pump concept: Potential biogeochemical significance in the globally changing ocean. Progress in Oceanography, 134, 432-450.
LI, W. K. W., DICKIE, P. M., IRWIN, B. D. & WOOD, A. M. 1992. Biomass of bacteria, cyanobacteria, prochlorophytes and photosynthetic eukaryotes in the Sargasso Sea. Deep Sea Research Part A, Oceanographic Research Papers, 39(3-4), 501-519.
LOGARES, R., DEUTSCHMANN, I. M., JUNGER, P. C., GINER, C. R., KRABBERØD, A. K., SCHMIDT, T. S., RUBINAT-RIPOLL, L., MESTRE, M., SALAZAR, G., RUIZ-GONZÁLEZ, C., SEBASTIÁN, M., VARGAS, C., ACINAS, S. G., DUARTE, C. M., GASOL, J. M. & MASSANA, R. 2020. Disentangling the mechanisms shaping the surface ocean microbiota. Microbiome, 8, 55.
LONGHURST, A. R. 2010. Ecological geography of the sea Amsterdam: Academic Press.
LOUCA, S., PARFREY, L. W. & DOEBELI, M. 2016. Decoupling function and taxonomy in the global ocean microbiome. Science, 353(6305), 1272-1277.
MALONE, T. C. & DUCKLOW, H. W. 1990. Microbial biomass in the coastal plume of Chesapeake Bay: Phytoplankton-bacterioplankton relationships. Limnology and Oceanography, 35(2), 296-312.
MANRIQUE, J. M. & JONES, L. R. 2017. Are ocean currents to slow to counteract SAR11 evolution? A next-generation sequencing, phylogeographic analysis. Molecular Phylogenetics and Evolution, 107, 324-337.
MARTÍNEZ-GARCÍA, S., FERNÁNDEZ, E., CALVO-DÍAZ, A., MARAÑÓN, E., MORÁN, X. A. G. & 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(5), 1701-1713.
MAZUECOS, I. P., ARÍSTEGUI, J., VÁZQUEZ-DOMÍNGUEZ, E., ORTEGA-RETUERTA, E., GASOL, J. M. & RECHE, I. 2015. Temperature control of microbial respiration and growth efficiency in the mesopelagic zone of the South Atlantic and Indian Oceans. Deep Sea Research Part I: Oceanographic Research Papers, 95, 131-138.
MCCLAIN, C. R., SIGNORINI, S. R. & CHRISTIAN, J. R. 2004. Subtropical gyre variability observed by ocean-color satellites. Deep Sea Research Part II: Topical Studies in Oceanography, 51(1-3), 281-301.
MCMANUS, G. B. & PETERSON, W. T. 1988. Bacterioplankton production in the nearshore zone during upwelling off central Chile. Marine Ecology Progress Series, 43(1-2), 11-17.
METZLER, P. M., GLIBERT, P. M., GAETA, S. A. & LUDLAM, J. M. 1997. New and regenerated production in the South Atlantic off Brazil. Deep Sea Research Part I: Oceanographic Research Papers, 44(3), 363-384.
MORÁN, X. A. G., ALONSO-SÁEZ, L., NOGUEIRA, E., DUCKLOW, H. W., GONZÁLEZ, N., LÓPEZ-URRUTIA, A., DÍAZ-PÉREZ, L., CALVO-DÍAZ, A., ARANDIA-GOROSTIDI, N. & HUETE-STAUFFER, T. M. 2015. More, smaller bacteria in response to ocean’s warming? Proceedings of the Royal Society B, 282(1810), 20150371.
MORRIS, R. M., FRAZAR, C. D. & CARLSON, C. A. 2012. Basin-scale patterns in the abundance of SAR11 subclades, marine Actinobacteria (OM1), members of the Roseobacter clade and OCS116 in the South Atlantic. Environmental Microbiology, 14(5), 1133-1144.
MORRIS, R. M., NUNN, B. L., FRAZAR, C., GOODLETT, D. R., TING, Y. S. & ROCAP, G. 2010. Comparative metaproteomics reveals ocean-scale shifts in microbial nutrient utilization and energy transduction. The ISME Journal, 4(5), 673-685.
MORRIS, R. M., RAPPÉ, M. S., CONNON, S. A., VERGIN, K. L., SIEBOLD, W. A., CARLSON, C. A. & GIOVANNONI, S. J. 2002. SAR11 clade dominates ocean surface bacterioplankton communities. Nature, 420(6917), 806-810.
OKSANEN, J., BLANCHET, F. G., KINDT, R., LEGENDRE, P., MINCHIN, P. R., O’HARA, R. B., SIMPSON, G. L., SOLYMOS, P., HENRY, M., STEVENS, H., WAGNER, H. & OKSANEN, M. J. 2013. Package ‘vegan’. Community Ecology Package, 2(9), 1-295.
OLSON, R. J., ZETTLER, E. R., CHISHOLM, S. W. & DUSENBERRY, J. A. 1991. Advances in oceanography through flow cytometry. In: DEMERS, S. (ed.). Particle analysis in oceanography. Berlin: NATO ASI Series, Series G, Ecological Sciences/Springer, pp. 351-399.
PALENIK, B., BRAHAMSHA, B., LARIMER, F. W., LAND, M., HAUSER, L., CHAIN, P., LAMERDIN, J., REGALA, W., ALLEN, E. E., MCCARREN, J., PAULSEN, I., DUFRESNE, A., PAQRTENSKY, F., WEBB, E. A. & WATERBURY, J. 2003. The genome of a motile marine Synechococcus. Nature, 424(6952), 1037-1042.
PARTENSKY, F., HESS, W. R. & VAULOT, D. 1999. Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiology and Molecular Biology Reviews, 63(1), 106-127.
PERNICE, M. C., FORN, I., GOMES, A., LARA, E., ALONSO-SÁEZ, L., ARRIETA, J. M., GARCIA, F. D. C., HERNANDO-MORALES, V., MACKENZIE, R., MESTRE, M., SINTES, E., TEIRA, E., VALENCIA, J., VARELA, M. M., VAQUÉ, D., DUARTE, C., GASOL, J. M. & MASSANA, R. 2015. Global abundance of planktonic heterotrophic protists in the deep ocean. The ISME Journal, 9(3), 782-792.
POMEROY, L. R. 1974. The ocean’s food web: a changing paradigm. BioScience, 24(9), 499-504.
POMEROY, L. R. & DEIBEL, D. 1986. Temperature regulation of bacterial activity during the spring bloom in Newfoundland coastal waters, Science, 233(4761), 359-361.
POMEROY, L. R., WILLIAMS, P. J. L., AZAM, F. & HOBBIE, J. E. 2007. The microbial loop. Oceanography, 20(2), 28-33.
PORTER, K. G. & FEIG, Y. S. 1980. The use of DAPI for identifying and counting aquatic microflora. Limnology and Oceanography, 25(5), 943-948.
RIBEIRO, C. G., MARIE, D., SANTOS, A. L., BRANDINI, F. P. & VAULOT, D. 2016. Estimating microbial populations by flow cytometry: comparison between instruments. Limnology and Oceanography, 14(11), 750-758.
RIBEIRO, C. G., SANTOS, A. L., MARIE, D., PELLIZARI, V. H., BRANDINI, F. P. & VAULOT, D. 2016. Pico and nanoplankton abundance and carbon stocks along the Brazilian Bight. PeerJ, 4, e2587.
RIVKIN, R. B. & LEGENDRE, L. 2001. Biogenic carbon cycling in the upper ocean: effects of microbial respiration. Science, 291(5512), 2398-2400.
ROCAP, G., LARIMER, F. W., LAMERDIN, J., MALFATTI, S., CHAIN, P., AHLGREN, N. A., ARELLANO, A., COLEMAN, M., HAUSER, L., HESS, W. R., JOHNSON, Z. I., LANDA, M., LINDELL, D., POST, A. F., REGALA, W., SHAH, M., SHAW, S. L., STEGLICH, C., SULLIVAN, M. B., TING, C. S., TOLONEN, A., WEBB, E. A., ZINSER, E. R. & CHISHOLM, S. W. 2003. Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature, 424(6952), 1042-1047.
RUSCH, D. B., HALPERN, A. L., SUTTON, G., HEIDELBERG, K. B., WILLIAMSON, S., YOOSEPH, S. & BEESON, K. 2007. The Sorcerer II global ocean sampling expedition: northwest Atlantic through eastern tropical Pacific. PLoS Biology, 5(3), e77.
SANZ-SÁEZ, I., SALAZAR, G., SÁNCHEZ, P., LARA, E., ROYO-LLONCH, M., SÀ, E. L., LUCENA, T., PUJALTE, M. J., VAQUÉ, D., DUARTE, C. M., GASOL, J. M., PEDRÓS-ALIÓ, C., SÁNCHEZ, O. & ACINAS, S. G. 2020. Diversity and distribution of marine heterotrophic bacteria from a large culture collection. BMC Microbiology, 20(1), 207.
SARMENTO, H., MONTOYA, J. M., VÁZQUEZ-DOMÍNGUEZ, E., VAQUÉ, D. & GASOL, J. M. 2010. Warming effects on marine microbial food web processes: how far can we go when it comes to predictions? Philosophical Transactions of the Royal Society B: Biological Sciences, 365(1549), 2137-2149.
SCHATTENHOFER, M., FUCHS, B. M., AMANN, R., ZUBKOV, M. V., TARRAN, G. A. & PERNTHALER, J. 2009. Latitudinal distribution of prokaryotic picoplankton populations in the Atlantic Ocean. Environmental Microbiology, 11(8), 2078-2093.
SERRET, P., FERNÁNDEZ, E. & ROBINSON, C. 2002. Biogeographic differences in the net ecosystem metabolism of the open ocean. Ecology, 83(11), 3225-3234.
SERRET, P., ROBINSON, C., ARANGUREN-GASSIS, M., GARCÍA-MARTÍN, E. E., GIST, N., KITIDIS, V., LOZANO, J., STEPHENS, J., HARRIS, C. & THOMAS, R. 2015. Both respiration and photosynthesis determine the scaling of plankton metabolism in the oligotrophic ocean. Nature Communications, 6(1), 1-10.
SERRET, P., ROBINSON, C., FERNÁNDEZ, E., TEIRA, E. & TILSTONE, G. 2001. Latitudinal variation of the balance between plankton photosynthesis and respiration in the eastern Atlantic Ocean. Limnology and Oceanography, 46(7), 1642-1652.
SIEBURTH, J. M., SMETACEK, V. & LENZ, J. 1978. Pelagic ecosystem structure: heterotrophic compartments of the plankton and their relationship to plankton size fractions. Limnology and Oceanography, 23(6), 1256-1263.
SIGNORINI, S. R., FRANZ, B. A. & MCCLAIN, C. R. 2015. Chlorophyll variability in the oligotrophic gyres: mechanisms, seasonality and trends. Frontiers in Marine Science, 2, 1.
SCHLITZER, R. 2020. Ocean data view (ODV) [online]. Available at: https://odv.awi.de [Accessed: 10 April 2021].
SUNAGAWA, S., ACINAS, S. G., BORK, P., BOWLER, C., EVEILLARD, D., GORSKY, G., GUIDI, L., IUDICONE, D., KARSENTI, E., LOMBARD, F., OGATA, H., PESANT, S., SULLIVAN, M. B., WINCKER P. & OGATA, H. 2020. Tara Oceans: towards global ocean ecosystems biology. Nature Reviews Microbiology, 18(8), 428-445.
SUNAGAWA, S., COELHO, L. P., CHAFFRON, S., KULTIMA, J. R., LABADIE, K., SALAZAR, G., DJAHANSCHIRI, B., ZELLER, G., MENDE, D. R., ALBERTI, A., CORNEJO-CASTILLO, F. M., COSTEA, P. I., CRUAUD, C., D’OVIDIO, F., ENGELEN, S., FERRERA, I., GASOL, J. M., GUIDI, L., HILDEBRAND, F., KOKOSZKA, F., LEPOIVRE, C., LIMA-MENDEZ, G., POULAIN, J., POULOS, B. T., ROYO-LLONCH, M., SARMENTO, H., VIEIRA-SILVA, S., DIMIER, C., PICHERAL M., SEARSON, S., KANDELS-LEWIS, S., BOWLER, C., VARGAS, C., GORSKY, G., GRIMSLEY, N., HINGAMP, S., SPIECH, S., STEMMANN, L., SULLIVAN, M. B., WEISSENBACH, J., WINCKER, P., KARSENTI, E., RAES, J., ACINAS, S. G. & BORK, P. 2015. Structure and function of the global ocean microbiome. Science, 348(6237), 1261359.
SUSINI-RIBEIRO, S. M., POMPEU, M., GAETA, S. A., SOUZA, J. S. & MASUDA, L. S. 2013. Topographical and hydrographical impacts on the structure of microphytoplankton assemblages on the Abrolhos Bank region, Brazil. Continental Shelf Research, 70, 88-96.
SWAN, B. K., CHAFFIN, M. D., MARTINEZ-GARCIA, M., MORRISON, H. G., FIELD, E. K., POULTON, N. J., DASHIELL, E., MASLAND, P., HARRIS, C. C., SZYRBA, A., CHAIN, P. S. G., KOREN, S., WOYKE, T. & STEPANAUSKAS, R. 2014. Genomic and metabolic diversity of Marine Group I Thaumarchaeota in the mesopelagic of two subtropical gyres. PloS One, 9(4), e95380.
TEIRA, E., MARTÍNEZ-GARCÍA, S., CALVO-DÍAZ, A. & MORÁN, X. A. G. 2010. Effects of inorganic and organic nutrient inputs on bacterioplankton community composition along a latitudinal transect in the Atlantic Ocean. Aquatic Microbial Ecology, 60(3), 299-313.
THOMAIDIS, N. S., GEORGIOU, C. A. & CALOKERINOS, A. C. 2004. Analytical chemistry in Balkan and East Mediterranean countries during 1994-2001. Analytica Chimica Acta, 505(1), 3-8.
THOMPSON, L. R., SANDERS, J. G., MCDONALD, D., AMIR, A., LADAU, J., LOCEY, K. J., PRILL, R. J., TRIPATHI, A., GIBBONS, S. M., ACKERMAN, G., NAVAS-MOLINA, J. A., JANSSEN, S., KOPULOVA, E., VÁZQUEZ-BAEZA, Y, HAROON, M. F., MORTON, J. T., MIRARAB, S., XU, Z. Z., HAROON, M. F., KANBAR, J., ZHU, Q., SONG, S. J., KOSCIOLEK, T., BOKULICH, N. A., LEFLER, J., BRISLAWN, C. J., HUMPHREY, G., OWENS, S. M., HAMPTON-MARCELL, J., BERG-LYONS, D., MCKENZIE, V., FIERER, N., FUHRMAN, J. A., CLAUSET, A., STEVENS, R. L., SHADE, A., POLLARD, K. S., GOODWIN, K. D., JANSSON, J. K., GILBERT, J. A., KINGHT, R. & NAVAS-MOLINA, J. A. 2017. A communal catalogue reveals Earth’s multiscale microbial diversity. Nature, 551(7681), 457-463.
TILSTONE, G. H., XIE, Y. Y., ROBINSON, C., SERRET, P., RAITSOS, D. E., POWELL, T., ARAGUREN-GASSIS, M., GARCIA-MARTIN, E. & KITIDIS, V. 2015. Satellite estimates of net community production indicate predominance of net autotrophy in the Atlantic Ocean. Remote Sensing of Environment, 164, 254-269.
TULLY, B. J., GRAHAM, E. D. & HEIDELBERG, J. F. 2018. The reconstruction of 2,631 draft metagenome-assembled genomes from the global oceans. Scientific Data, 5(1), 170203.
VÁZQUEZ-DOMÍNGUEZ, E., DUARTE, C. M., AGUSTÍ, S., JÜRGENS, K., VAQUÉ, D. & GASOL, J. M. 2008. Microbial plankton abundance and heterotrophic activity across the Central Atlantic Ocean. Progress in Oceanography, 79(1), 83-94.
WATSON, S. W., NOVITSKY, T. J., QUINBY, H. L. & VALOIS, F. W. 1977. Determination of bacterial number and biomass in the marine environment. Applied and Environmental Microbiology, 33(4), 940-947.
WESTBERRY, T. K., WILLIAMS, P. J. L. B. & BEHRENFELD, M. J. 2012. Global net community production and the putative net heterotrophy of the oligotrophic oceans. Global Biogeochemical Cycles, 26(4), GB4019.
WHITMAN, W. B., COLEMAN D. C. & WIEBE, W. J. 1998. Prokaryotes: the unseen majority. Proceedings of the National Academy of Sciences of the U.S.A., 95(12), 6578-6583.
WILLIAMS, P. J. B. 1981. Microbial contribution to overall marine plankton metabolism-direct measurements of respiration. Oceanologica Acta, 4(3), 359-364.
WILLIAMS, P. J. B. 1998. The balance of plankton respiration and photosynthesis in the open oceans. Nature, 394(6688), 55-57.
WILLIAMS, P. J. B., QUAY, P. D., WESTBERRY, T. K. & BEHRENFELD, M. J. 2013. The oligotrophic ocean is autotrophic. Annual Review of Marine Science, 5, 535-549.
WOHLERS, J., ENGEL, A., ZÖLLNER, E., BREITHAUPT, P., JÜRGENS, K., HOPPE, H. G., SOMMER, U. & RIEBESELL, U. 2009. Changes in biogenic carbon flow in response to sea surface warming. Proceedings of the National Academy of Sciences of the U.S.A., 106(17), 7067-7072.
WORDEN, A. Z., FOLLOWS, M. J., GIOVANNONI, S. J., WILKEN, S., ZIMMERMAN, A. E. & KEELING, P. J. 2015. Environmental science. Rethinking the marine carbon cycle: factoring in the multifarious lifestyles of microbes. Science, 347(6223), 1257594.
YENTSCH, C. M., HORAN, P. K., MUIRHEAD, K., DORTCH, Q., HAUGEN, E., LEGENDRE, L., MURPHY, L. S., PERRY, M. J., PHINNEY, D. A., POMPONI, S. A., SPINRAD, R. W. & WO, M. 1983. Flow cytometry and cell sorting: a technique for analysis and sorting of aquatic particles. Limnology and Oceanography, 28(6), 1275-1280.
ZHANG, F., LIU, J., LI, Q., ZOU, L. & ZHANG, Y. 2016. The research of typical microbial functional group reveals a new oceanic carbon sequestration mechanism—a case of innovative method promoting scientific discovery. Science China Earth Sciences, 59(3), 456-463.
ZHANG, Y., ZHAO, M., CUI, Q., FAN, W., QI, J., CHEN, Y., ZHANG, Y. Y., GAO, K., FAN, J. F., WANG, G. Y., YAN, C. L., LU, H. L., LUO, Z. L., ZHANG, Z. L., ZHENG, Q., XIAO, W. & JIAO, N. Z. 2017. Processes of coastal ecosystem carbon sequestration and approaches for increasing carbon sink. Science China Earth Sciences, 60(5), 809-820.
ZUBKOV, M. V., SLEIGH, M. A. & BURKILL, P. H. 2000. Assaying picoplankton distribution by flow cytometry of underway samples collected along a meridional transect across the Atlantic Ocean. Aquatic Microbial Ecology, 21(1), 13-20.
ZUBKOV, M. V., SLEIGH, M. A., BURKILL, P. H. & LEAKEY, R. J. 2000a. Picoplankton community structure on the Atlantic Meridional Transect: a comparison between seasons. Progress in oceanography, 45(3-4), 369-386.
ZUBKOV, M. V., SLEIGH, M. A., BURKILL, P. H. & LEAKEY, R. J. 2000b. Bacterial growth and grazing loss in contrasting areas of North and South Atlantic. Journal of Plankton Research, 22(4), 685-711.
ZUBKOV, M. V., SLEIGH, M. A., TARRAN, G. A., BURKILL, P. H. & LEAKEY, R. J. 1998. Picoplanktonic community structure on an Atlantic transect from 50°N to 50°S. Deep Sea Research Part I: Oceanographic Research Papers, 45(8), 1339-1355.
