Register      Login
Environmental Chemistry Environmental Chemistry Society
Environmental problems - Chemical approaches
Shopping Cart: ( empty )
You are here: Home > Journals > EN > EN07081
RESEARCH ARTICLE
Contents Vol 5(2)

Macro and micro nutrient limitation of microbial productivity in oligotrophic subtropical Atlantic waters

Joanna L. Dixon
+ Author Affiliations
- Author Affiliations

Plymouth Marine Laboratory, Prospect Place, West Hoe, Plymouth, Devon PL1 3DH, UK. Email: jod@pml.ac.uk

Environmental Chemistry 5(2) 135-142 https://doi.org/10.1071/EN07081
Submitted: 29 October 2007  Accepted: 14 March 2008   Published: 17 April 2008

Environmental context. The subtropical oceans comprise ~70% of the world’s ocean surface and profoundly affect global biogeochemistry and climate. They are characteristically low-nutrient regions, but, owing to their large extent and often rapid nutrient turnover, may contribute to greater than 30% of the total marine primary production. However, there remains long-standing uncertainty as to what individual or combination of resources, e.g. macro (N, P) and micro (trace metals) nutrients, limit or co-limit marine productivity and thus total carbon fixation in these spatially dominant gyre systems.

Abstract. The subtropical oceans are characteristically low-nutrient low-chlorophyll regions, but owing to their geographical dominance and rapid nutrient cycling may contribute >30% of the total marine primary production. The present study investigates the addition of P, Fe, Co and Zn on rates of primary production and heterotrophic bacterial production, through a combination of mesoscale in situ (P, and P + Fe) and in vitro (Co or Zn) bioassay incubation experiments.

Results from the bioassay incubation experiments suggest that primary production and chlorophyll a biomass are limited by N and P in this oligotrophic region. However, both were increased further after addition of trace metal micronutrients in the order Fe + Zn ≥ Fe + Co > Fe ≈ Co. In contrast, rates of heterotrophic bacterial production did not appear to be P, or significantly, P + Fe limited, although in situ rates did increase during the first 12 h of mesoscale P fertilisation (which were not mirrored in the mesoscale P + Fe addition). The addition of Co to unfertilised waters increased heterotrophic bacterial production and the numbers of heterotrophic bacteria, Prochlorococcus spp. and Synechococcus spp., suggesting Co limitation. Prochlorococcus spp. were the most abundant autotrophs. The highest increases in both heterotrophic and autotrophic carbon assimilation were shown after in vitro addition of either Co or Zn to mesoscale enriched P + Fe waters, suggesting multiple limitation of microbial growth rates in the subtropical oligotrophic north-east Atlantic.

Additional keywords: cyanobacteria, heterotrophic bacterial production, mesoscale P and P + Fe fertilisation, primary production.


Acknowledgements

I wish to thank the entire Feep group including the Fe/P/SF6 release and tracking teams, the crew and officers of RV Poseidon and RRS Charles Darwin, Dr I. Joint, Professor N. J. P. Owens, Dr P. D. Nightingale and Dr A. P. Rees. In addition, I would like to thank E. M. S. Woodward and J. Stephens for the nutrient data, G. A. Tarran for the flow cytometry data, D. Clark for the ammonium data, E. Fileman and V. Collins for the microzooplankton biomass data, S. Kimmance for the herbivory data and S. Ussher for the dissolved Fe data. The present work was funded by the Plymouth Marine Laboratory core research program 2001–2006.


References


[1]   P. G. Falkowski , R. T. Barber , V. Smetacek , Biogeochemical controls and feedbacks on ocean primary production. Science 1998 , 281,  200.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[2]   M. M. Mills , C. Ridame , M. Davey , J. La Roche , R. J. Geider , Iron and phosphorus co-limit nitrogen fixation in the eastern tropical North Atlantic. Nature 2004 , 429,  292.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[3]   F. M. M. Morel , N. M. Price , The biogeochemical cycles of trace metals in the oceans. Science 2003 , 300,  944.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[4]   J. Wu , W. Sunda , E. A. Boyle , D. M. Karl , Phosphate depletion in the Western North Atlantic Ocean. Science 2000 , 289,  759.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[5]   P. G. Falkowski , Evolution of the nitrogen cycle and its influence on the biological sequestration of CO2 in the ocean. Nature 1997 , 387,  272.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[6]   S. A. Sanudo-Wilhelmy , A. B. Kustka , C. J. Gobler , D. A. Hutchins , M. Yang , K. Lwiza , J. Burns , D. G. Capone , J. A. Raven , E. J. Carpenter , Phosphorus limitation of nitrogen fixation by Trichodesmium in the central Atlantic Ocean. Nature 2001 , 411,  66.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[7]   D. M. Karl , R. Letelier , L. Tupas , J. Dore , J. Christian , D. Hebel , The role of nitrogen fixation in biogeochemical cycling in the subtropical North Pacific Ocean. Nature 1997 , 388,  533.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[8]   B. C. Cho , F. Azam , Major role of bacteria in biogeochemical fluxes in the ocean’s interior. Nature 1988 , 332,  441.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[9]   P. D. Tortell , M. T. Maldonado , J. Granger , N. M. Price , Marine bacteria and biogeochemical cycling of iron in the oceans. FEMS Microbiol. Ecol. 1999 , 29,  1.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[10]   M. S. Hale , R. B. Rivkin , P. Matthews , N. S. R. Agawin , W. K. W. Li , Microbial response to a mesoscale iron enrichment in the NE subarctic Pacific: heterotrophic bacterial processes. Deep-Sea Res. II 2006 , 53,  2231.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[11]   T.-Y. Ho , A. Quigg , Z. V. Finkel , A. J. Milligan , K. Wyman , P. G. Falkowski , F. M. M. Morel , The elemental composition of some marine phytoplankton. J. Phycol. 2003 , 39,  1145.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[12]   J. L. Dixon , P. J. Statham , C. E. Widdicombe , R. M. Jones , S. Barquero-Molina , B. Dickie , M. Nimmo , C. M. Turley , Cadmium uptake by marine micro-organisms in the English Channel and Celtic Sea. Aquat. Microb. Ecol. 2006 , 44,  31.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[13]   B. L. Vallee , D. S. Auld , Zinc coordination, function and structure of zinc enzymes and other proteins. Biochem 1990 , 29,  5647.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[14]   Y. Shaked , Y. Xu , K. Leblanc , F. M. M. Morel , Zinc availability and alkaline phosphatase activity in Emiliania huxleyi: implications for Zn–P co-limitation in the ocean. Limnol. Oceanogr. 2006 , 51,  299.
         open url image1

[15]   W. G. Sunda , S. A. Huntsman , Cobalt and zinc interreplacement in marine phytoplankton: biological and geochemical implications. Limnol. Oceanogr. 1995 , 40,  1404.
         open url image1

[16]   M. A. Saito , J. W. Moffett , S. W. Chisholm , J. B. Waterbury , Cobalt limitation and uptake in Prochlorococcus. Limnol. Oceanogr. 2002 , 47,  1629.
         open url image1

[17]   A. F. Carlucci , P. M. Bowes , Vitamin B12, thiamine and biotin contents of marine phytoplankton. J. Phycol. 1972 , 8,  133.
         open url image1

[18]   D. G. Swift , W. R. Taylor , Growth of vitamin B12-limited cultures: Thalassiosira pseudonana, Monochrysis lutheri and Isochrysis galbana. J. Phycol. 1974 , 10,  385.
         open url image1

[19]   M. Kobayashi , S. Shimizu , Cobalt proteins. Eur. J. Biochem. 1999 , 261,  1.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[20]   M. T. Croft , A. D. Lawrence , E. Raux-Deery , M. J. Warren , A. G. Smith , Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 2005 , 438,  90.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[21]   A. Longhurst , S. Sathyendranath , T. Platt , C. Caverhill , An estimate of global primary production in the ocean from satellite radiometer data. J. Plankton Res. 1995 , 17,  1245.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[22]   R. C. Upstill-Goddard , A. J. Watson , J. Wood , M. I. Liddicoat , Sulphur hexafluoride and 3He as seawater tracers – deployment techniques and continuous underway analysis for sulphur hexafluoride. Anal. Chim. Acta 1991 , 249,  555.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[23]   P. D. Nightingale , G. Malin , C. S. Law , A. J. Watson , P. S. Wood , M. I. Liddicoat , J. Boutin , R. C. Upstill-Goddard , In situ evaluation or air–sea gas exchange parameterizations using novel conservative and volatile tracers. Global Biogeochem. Cycles 2000 , 14,  373.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[24]   C. S. Law , A. J. Watson , M. I. Liddicoat , Automated vacuum analysis of sulphur hexafluoride in seawater: derivation of the atmospheric trend (1970–1993) and potential as a transient tracer. Mar. Chem. 1994 , 48,  57.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[25]   M. V. Zubkov , M. A. Sleigh , P. H. Burkhill , R. J. G. Leakey , Picoplankton community structure on the Atlantic Meridional Transect: a comparison between seasons. Prog. Oceanogr. 2000 , 45,  369.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[26]   I. Joint , A. Pomroy , Phytoplankton biomass and production in the southern North Sea. Mar. Ecol. Prog. Ser. 1993 , 99,  169.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[27]   D. C. Smith , F. Azam , A simple, economical method for measuring bacterial protein synthesis rates in seawater using 3H-leucine. Mar. Microb. Food Webs 1992 , 6,  107.
         open url image1

[28]   A. R. Bowie , E. P. Achterberg , R. F. C. Mantoura , P. J. Worsfold , Determination of sub-nanomolar levels of iron in seawater using flow injection with chemiluminescence detection. Anal. Chim. Acta 1998 , 361,  189.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[29]   E. M. S. Woodward , Nanomolar detection for phosphate and nitrate using liquid waveguide technology. EOS Trans. (AGU Suppl.) 2002 , 83,  92.
         open url image1

[30]   E. M. S. Woodward , A. P. Rees , Nutrient distributions in an anticyclonic eddy in the north-east Atlantic Ocean, with reference to nanomolar ammonium concentrations. Deep-Sea Res. II 2001 , 48,  775.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[31]   Cullen J. J., Yang X., Macintyre H. L., Nutrient limitation of marine photosynthesis, in Primary Productivity and Biogeochemical Cycles in the Sea (Eds P. G. Falkowski, A. D. Woodhead) 1992 (Plenum: New York).

[32]   M. A. Saito , T. J. Goepfert , J. T. Ritt , Some thoughts on the concept of colimitation: three definitions and the importance of bioavailabilty. Limnol. Oceanogr. 2008 , 53,  276.
         open url image1

[33]   L. M. Graziano , R. J. Geider , W. K. W. Li , M. Olaizola , Nitrogen limitation of North Atlantic phytoplankton: analysis of physiological condition in nutrient enrichment experiments. Aquat. Microb. Ecol. 1996 , 11,  53.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[34]   L. Alonso-Sáez , J. M. Gasol , J. Aristegui , J. C. Vilas , D. Vaqué , C. M. Duarte , S. Agusti , Large-scale variability in surface bacterial carbon demand and growth efficiency in the subtropical north-east Atlantic Ocean. Limnol. Oceanogr. 2007 , 52,  533.
         open url image1

[35]   X. A. G. Moran , E. Fernández , V. Pérez , Size fractionated primary production, bacterial production and net community production in subtropical and tropical domains of the oligotrophic NE Atlantic in autumn. Mar. Ecol. Prog. Ser. 2004 , 274,  17.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[36]   F. Partensky , J. Blanchot , F. Lantoine , J. Neveux , D. Marie , Vertical structure of picophytoplankton at different trophic sites of the tropical north-eastern Atlantic Ocean. Deep-Sea Res. I 1996 , 43,  1191.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[37]   M. V. Zubkov , M. A. Sleigh , G. A. Tarran , P. H. Burkhill , R. J. G. Leakey , Picoplankton community structure on an Atlantic transect from 50°N to 50°S. Deep-Sea Res. I 1998 , 45,  1339.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[38]   S. Psarra , T. Zohary , M. D. Krom , R. F. C. Mantoura , T. Polychronaki , N. Stambler , T. Tanaka , A. Tselepides , T. F. Thingstad , Phytoplankton response to a Lagrangian phosphate addition in the Levantine Sea (Eastern Mediterranean). Deep-Sea Res. II 2005 , 52,  2944.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[39]   Goldman J. C., Physiological processes, nutrient availability, and the concept of relative growth rate in marine phytoplankton ecology, in Primary Productivity in the Sea (Ed. P. G. Falkowski) 1980 (Plenum: New York).

[40]   D. J. Gifford , Impact of grazing by microzooplankton in the North-west arm of Halifax Harbour, Nova Scotia. Mar. Ecol. Prog. Ser. 1988 , 47,  249.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[41]   E. J. Lessard , M. C. Murrell , Microzooplankton herbivory and phytoplankton growth in the north-western Sargasso Sea. Aquat. Microb. Ecol. 1998 , 16,  173.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[42]   A. P. Rees , E. M. S. Woodward , I. Joint , Concentrations and uptake of nitrate and ammonium in the Atlantic Ocean between 60°N and 50°S. Deep-Sea Res. II 2006 , 53,  1649.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[43]   T. Zohary , B. Herut , M. D. Krom , R. F. C. Mantoura , P. Pitta , S. Psarra , F. Rassoulzadegan , N. Stambler , T. Tanaka , T. F. Thingstad , E. M. S. Woodward , P-limited bacteria and N and P co-limited phytoplankton in the Eastern Mediterranean – a microcosm experiment. Deep-Sea Res. II 2005 , 52,  3011.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[44]   C. M. Moore , M. M. Mill , R. Langlois , A. Milne , E. P. Achterberg , J. La Roche , R. J. Geider , Relative influence of nitrogen and phosphorus availability on phytoplankton physiology and productivity in the oligotrophic subtropical North Atlantic Ocean. Limnol. Oceanogr. 2008 , 53,  291.
         open url image1

[45]   L. R. Moore , A. F. Post , G. Rocap , S. W. Chisholm , Utilization of different nitrogen sources by the marine cyanobacteria Prochlorococcus and Synechococcus. Limnol. Oceanogr. 2002 , 47,  989.
         open url image1

[46]   M. A. Saito , G. Rocap , J. W. Moffett , Production of cobalt-binding ligands in a Synechococcus feature at the Costa Rica upwelling dome. Limnol. Oceanogr. 2005 , 50,  279.
         open url image1

[47]   Wackett L. P., Orme-Johnson W. H., Walsh C. T., Transition metal enzymes in bacterial metabolism, in Metal Ions and Bacteria (Eds T. J. Beveridge, R. J. Doyle) 1989 (Wiley: New York).

[48]   R. J. Chróst , J. Overbeck , Kinetics of alkaline phosphatase activity and phosphorus availability for phytoplankton and bacterioplankton in Lake Plußsee (North German eutrophic lake). Microb. Ecol. 1987 , 13,  229.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[49]   J. Martinez , D. C. Smith , G. F. Steward , F. Azam , Variability in ectohydrolytic enzyme activities of pelagic marine bacteria and its significance for substrate processing in the sea. Aquat. Microb. Ecol. 1996 , 10,  223.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[50]   Chróst R. J., Microbial ectoenzymes in aquatic environments, in Aquatic Microbial Ecology: Biochemical and Molecular Approaches (Eds J. Overbeck, R. J. Chróst) 1990 (Springer-Verlag: New York).

[51]   J. W. Ammerman , F. Azam , Bacterial 5′-nucleotidase in aquatic ecosystems: a novel mechanism of phosphorus regeneration. Science 1985 , 227,  1338.
        | Crossref | GoogleScholarGoogle Scholar | PubMed |  open url image1

[52]   M. J. Ellwood , C. M. G. Van den berg , Determination of organic complexation of cobalt in seawater by cathodic stripping voltammetry. Mar. Chem. 2001 , 75,  33.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[53]   W. G. Sunda , S. A. Hunstman , Feedback interactions between zinc and phytoplankton in seawater. Limnol. Oceanogr. 1992 , 37,  25.
         open url image1

[54]   M. J. Ellwood , C. M. G. Van den berg , Zinc speciation in the north-eastern Atlantic Ocean. Mar. Chem. 2000 , 68,  295.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[55]   D. W. Crawford , M. S. Lipsen , D. A. Purdie , M. C. Lohan , P. J. Statham , F. A. Whitney , J. N. Putland , W. K. Johnson , N. Sutherland , T. D. Peterson , P. J. Harrison , C. S. Wong , Influence of zinc and iron enrichments on phytoplankton growth in the north-eastern subarctic Pacific. Limnol. Oceanogr. 2003 , 48,  1583.
         open url image1

[56]   K. Kremling , P. Streu , The behaviour of dissolved Cd, Co, Zn, and Pb in North Atlantic near-surface waters (30°N/60°W–60°N/2°W). Deep-Sea Res. I 2001 , 48,  2541.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1