Skip to main content

The role of iron in the bacterial degradation of organic matter derived from Phaeocystis antarctica

Abstract

In high-nutrient low-chlorophyll areas, bacterial degradation of organic matter may be iron-limited. The response of heterotrophic bacteria to Fe addition may be directly controlled by Fe availability and/or indirectly controlled through the effect of enhanced phytoplankton productivity and the subsequent supply of organic matter suitable for bacteria. In the present study, the role of Fe on bacterial carbon degradation was investigated through regrowth experiments by monitoring bacterial response to organic substrates derived from Phaeocystis antarctica cultures set up in <1 nM Fe (LFe) and in Fe-amended (HFe) Antarctic seawater. Results showed an impact of Fe addition on the morphotype dominance (colonies vs. single cells) of P. antarctica and on the quality of Phaeocystis-derived organic matter. Fe addition leaded to a decrease of C/N ratio of Phaeocystis material. The bacterial community composition was modified as observed from denaturing gradient gel electrophoresis (DGGE) profiles in LFe as compared to HFe bioassays. The percentage of active bacteria as well as their specific metabolic activities (ectoenzymatic hydrolysis, growth rates and bacterial growth efficiency) were enhanced in HFe bioassays. As a consequence, the lability of Phaeocystis-derived organic matter was altered, i.e., after seven days more than 90% was degraded in HFe and only 9% (dissolved) and 55% (total) organic carbon were degraded in LFe bioassays. By inducing increased bacterial degradation and preventing the accumulation of dissolved organic carbon, the positive effect of Fe supply on the carbon biological pump may partly be counteracted.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Ammerman JW, Fuhrman JA, Hagström Å, Azam F (1984) Bacterioplankton growth in seawater. I. Growth kinetics and cellular characteristics in seawater culture. Mar Ecol Prog Ser 18:31–39

    Google Scholar 

  • Arrieta JM, Weinbauer MG, Lute C, Herndl GJ (2004) Response of bacterioplankton to iron fertilization in the Southern Ocean. Limnol Oceanogr 49(3):799–808

    Article  Google Scholar 

  • Baumann MEM, Lancelot C, Brandini FP, Sakshaug E, John DM (1994) The taxonomic identity of the cosmopolitan prymnesiophyte Phaeocystis: a morphological and ecophysiological approach. J Mar Syst 5:5–22

    Article  Google Scholar 

  • Becquevort S, Smith WO Jr (2001) Aggregation, sedimentation and biodegradability of phytoplankton-derived material during spring in the Ross Sea, Antarctica. Deep-Sea Res II 48:4155–4178

    Article  Google Scholar 

  • Bölter M, Dawson R (1982) Heterotrophic utilization of biochemical compounds in Antarctic waters. Neth J Sea Res 16:315–332

    Article  Google Scholar 

  • Carlson CA, Ducklow HW, Smith WO, Hansel DA (1998) Carbon dynamics during spring blooms in the Ross Sea polynya and the Sargasso Sea: contrasts in dissolved and particulate organic carbon portioning. Limnol Oceanogr 43:375–386

    Article  Google Scholar 

  • Carlson CA, Bates NR, Ducklow HW, Hansell DA (1999) Estimation of bacterial respiration and growth efficiency in the Ross Sea, Antarctica. Aquat Microb Ecol 19:229–244

    Google Scholar 

  • Cherrier J, Bauer JE, Druffel ERM (1996) Utilization and turnover of labile dissolved organic matter by bacterial heterotrophs in eastern North Pacific surface waters. Mar Ecol Prog Ser 139:267–279

    Google Scholar 

  • Christian JR, Karl DM (1995) The bacterial ectoenzyme activities in marine waters: activity ratios and temperature responses in three oceanographic provinces. Limnol Oceanogr 40:1042–1049

    Article  Google Scholar 

  • Church MJ, Hutchins DA, Ducklow HW (2000) Limitation of bacterial growth by dissolved organic matter and iron in the Southern Ocean. Appl Environ Microbiol 66:455–466

    Article  Google Scholar 

  • Coale KH, Wang X, Tanner SJ, Johnson KS (2003) Phytoplankton growth and biological response to iron and zinc addition in the Ross Sea and Antarctic Circumpolar Current along 170°W. Deep Sea Res II 50:635–653

    Article  Google Scholar 

  • Cochlan WP (2001) The heterotrophic bacterial response during a mesoscale iron enrichment experiment (IronEx II) in the eastern Equatorial Pacific Ocean. Limnol Oceanogr 46:428–435

    Article  Google Scholar 

  • Davidson AT, Marchant HJ (1992) Protists abundance and carbon concentration during a Phaeocystis-dominated bloom at an Antarctic coastal site. Polar Biol 12:387–395

    Article  Google Scholar 

  • de Baar HJW, Boyd PW, Coale KH, Landry MR, Tsuda A, Assmy P, Bakker DCE, Bozec Y, Barber RT, Brzezinski MA, Buesseler KO, Boye M, Croot PL, Gervais F, Gorbunov MY, Harrison PJ, Hiscock WT, Laan P, Lancelot C, Law CS, Levasseur M, Marchetti A, Millero FJ, Nishioka J, Nojiri Y, van Oijen T, Riebesell U, Rijkenberg MJA, Saito H, Takeda S, Timmermans KR, Veldhuis MJW, Waite AM, Wong C (2005) Synthesis of iron fertilization experiments: from the iron age in the age of enlightenment. J Geophys Res 110, C09S16. DOI: 10.1029/2004JC002601

  • Ducklow H (2000) Bacterial production and biomass in the oceans. In: Kirchman DL (ed) Microbial ecology of the oceans. Wiley, New-York, pp 85–120

    Google Scholar 

  • Ducklow HW, Carlson CA, Smith WO (1999) Bacterial growth in experimental plankton assemblages and seawater cultures from the P. antarctica bloom in the Ross Sea, Antarctica. Aquat Microb Ecol 19:215–227

    Google Scholar 

  • Eberlein K, Leal MT, Hammer KD, Hickel W (1985) Dissolved organic substances during a Phaeocystis pouchetii bloom in the German Bight (North Sea). Mar Biol 89:31l–316

    Article  Google Scholar 

  • El-Sayed SZ, Biggs DC, Holm-Hansen O (1983) Phytoplankton standing crop, primary productivity, and near surface nitrogenous nutrient fields in the Ross Sea, Antarctica. Deep-Sea Res 30:871–886

    Article  Google Scholar 

  • Fogg GE (1983) The ecological significance of extracellular products of phytoplankton photosynthesis. Bot Mar 256:3–14

    Article  Google Scholar 

  • Furhman JA, Azam F (1982) Thymidine incorporation as a measure of heterotrophic bacterioplankton production in marine surface waters: evaluation and field results. Mar Biol l66:109–120

    Article  Google Scholar 

  • Geider RJ, LaRoche J (2002) Redfield revisited: variability of C:N:P in marine microalgae and its biochemical basis. Eur J Phycol 37:1–17

    Article  Google Scholar 

  • Gerringa LJA, de Baar HJW, Timmermans KR (2000) A comparison of iron limitation of phytoplankton in natural oceanic waters and laboratory media conditioned with EDTA. Mar Chem 68:335–346

    Article  Google Scholar 

  • Giovannoni SJ, Sting U (2005) Molecular diversity and ecology of microbial plankton. Nature 437:343–347

    Article  Google Scholar 

  • Gobler CJ, Hutchins DA, Fisher NS, Cosper EM, Sanùdo-Wilhelmy SA (1997) Release and bioavailability of C, N, P, Fe, and Se following viral lysis of a marine chrysophyte. Limnol Oceanogr 42:1492–1504

    Article  Google Scholar 

  • Granger J, Price NM (1999) The importance of siderophores in iron nutrition of heterotrophic marine bacteria. Limnol Oceanogr 44:541–555

    Article  Google Scholar 

  • Hall JA, Safi K (2001) The impact of in situ Fe fertilisation on the microbial food web in the Southern Ocean. Deep-Sea Res II 48:2591–2613

    Article  Google Scholar 

  • Hutchins DA, DiTullio GR, Zhang Y, Bruland W (1998) An iron limitation mosaic in the California upwelling regime. Limnol Oceanogr 43:1037–1054

    Article  Google Scholar 

  • Hutchins DA, Campbell BJ, Cottrell MT, Takeda S (2001) Response of marine bacterial community composition to iron additions in three iron-limited regimes. Limnol Oceanogr 46(6):1535–1545

    Article  Google Scholar 

  • Kirchman DL (2000) Uptake and regeneration of inorganic nutrients by marine heterotrophic bacteria. In: Kirchman DL (ed) Microbial ecology of the oceans. Wiley, New-York, pp 261–288

    Google Scholar 

  • Kirchman DL, Meon B, Cottrell MT, Hutchins DA (2000) Carbon versus iron limitation of bacterial growth in the California upwelling regime. Limnol Oceanogr 45(8):1681–1688

    Article  Google Scholar 

  • Kirchman DL, Hoffman KA, Weaver R, Hutchins DA (2003) Regulation of growth and energetics of a marine bacterium by nitrogen source and iron availability. Mar Ecol Progr Ser 250:291–296

    Google Scholar 

  • Koroleff F (1983a) Determination of ammonia. In: Grasshoff K, Ehrhardt M, Kremling K (eds) Methods of seawater analysis. Verlag-Chemie, Basel, pp 150–157

    Google Scholar 

  • Koroleff F (1983b) Determination of phosphorus. In: Grasshoff K, Ehrhardt M, Kremling K (eds) Methods of seawater analysis. Verlag-Chemie, Basel, pp 125–139

    Google Scholar 

  • Kudo I, Miyamoto M, Noiri Y, Maita Y (2000) Combined effects of temperature and iron on the growth and physiology of the marine diatom Phaeodactylum tricornutum (Bacillariophyceae). J Phycol 36(6):1096–1102

    Article  Google Scholar 

  • Lancelot C (1983) Factors affecting phytoplankton extracellular release in the Southern Bight of the North Sea. Mar Ecol Prog Ser 12:115–121

    Google Scholar 

  • Lancelot C, Mathot S, Owens NJP (1986) Modelling protein synthesis, a step to an accurate estimate of net primary production: the case of Phaeocystis pouchetii colonies in Belgian coastal waters. Mar Ecol Prog Ser 32:193–202

    Google Scholar 

  • Lancelot C, Billen G, Sournia A, Weisse T, Colijin F, Veldhuis MJW, Davies A, Wassman P (1987) Phaeocystis blooms and nutrient enrichment in the continental coastal zones of the North Sea. AMBIO 16(1):38–46

    Google Scholar 

  • Lewandowska J, Kosakowska A (2004) Effect of iron limitation on cells of the diatom Cyclotella meneghiniana Kützing. Oceanologia 46(2):269–287

    Google Scholar 

  • Lowther WT, Matthews BW (2000) Structure and function of the methionine aminopeptidases. Biochim Biophys Acta 1477:157–167

    Google Scholar 

  • Mathot S, Smith WO Jr, Carlson CA, Garrison DL (2000) Estimate of Phaeocystis sp. carbon biomass: methodological problems related to the mucilaginous nature of the colonial matrix. J Phycol 36:1049–1056

    Article  Google Scholar 

  • Muggli DL, Lecourt M, Harrison PJ (1996) Effects of iron and nitrogen source on the sinking rate, physiology and metal composition of an oceanic diatom from the subarctic Pacific. Mar Ecol Prog Ser 132:215–227

    Google Scholar 

  • Nagata T (2000) Production mechanisms of dissolved organic matter. In: Kirchman L (ed) Microbial ecology of the oceans. Wiley, New York, pp 121–152

    Google Scholar 

  • Obata H, Karatani H, Nakayama E (1993) Automated determination of iron in seawater by chelating resin concentration and chemiluminescence detection. Anal Chem 5:1524–1528

    Article  Google Scholar 

  • Oliver JL, Barber RT, Smith WO, Ducklow HW (2004) The heterotrophic bacterial response during the southern ocean iron experiment (SOFeX). Limnol Oceanogr 49:2129–2140

    Article  Google Scholar 

  • Pakulski JD, Coffin RB, Kelley CA, Holder SL, Downer R, Aas DP, Lyons MM, Jeffrey WH (1996) Iron stimulation of Antarctic bacteria. Nature 383:133–143

    Article  Google Scholar 

  • Pomeroy LR, Wiebe WJ, Deibel D, Thompson RJ, Rowe GT, Pakulski JD (1991) Bacterial responses to temperature and substrate concentration during the Newfoundland spring bloom. Mar Ecol Prog Ser 75:143–159

    Article  Google Scholar 

  • Poorvin L, Rinta-Kanto JM, Hutchins SW, Wilhem SW (2004) Viral release of iron and its bioavailability to marine plankton. Limnol Oceanogr 49:1734–1741

    Article  Google Scholar 

  • Porter KG, Feig YS (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25:943–948

    Article  Google Scholar 

  • Price NM, Ahner BA, Morel FMM (1994) The equatorial Pacific ocean: grazer controlled phytoplankton populations in an iron-limited ecosystem. Limnol Oceanogr 39:520–534

    Article  Google Scholar 

  • Raven J (1988) The iron and molybdenum use efficiencies of plant growth with different energy, carbon and nitrogen sources. New Phytol 109:279–287

    Article  Google Scholar 

  • Redfield AC, Ketchum BH, Richards FA (1963) The influence of organisms on the composition of seawater. In: Hill MN (ed) The sea. Wiley, New York, pp 26–77

    Google Scholar 

  • Rodriguez GG, Phipps D, Ishiguro K, Ridgeway HF (1992) Use of fluorescent redox probe for direct visualization of actively respiring bacteria. Appl Environ Microbiol 58:1801–1808

    Google Scholar 

  • Sarthou G, Baker AR, Blain S, Achterberg EP, Boye M, Bowie AR, Croot P, Laan P, de Baar HJW, Jickells TD, Worsfold PJ (2003) Atmospheric iron deposition and sea-surface dissolved iron concentrations in the eastern Atlantic Ocean. Deep-Sea Res 50:1339–1352

    Article  Google Scholar 

  • Schäfer H, Muyzer G (2001) Denaturing gradient gel electrophoresis in marine microbial ecology. In: Paul J (ed) Methods in microbiology, vol 30. Academic Press, London, pp 425–468

  • Schoemann V, Wollast R, Chou L, Lancelot C (2001) Effects of photosynthesis on the accumulation of Mn and Fe by Phaeocystis colonies. Limnol Oceanogr 46:1065–1076

    Article  Google Scholar 

  • Schoemann V, Becquevort S, Stefels J, Rousseau V, Lancelot C (2005) Phaeocystis blooms in the global ocean and their controlling mechanisms: a review. J Sea Res 53:43–66

    Article  Google Scholar 

  • Schumann R, Rieling T, Görs S, Hammer A, Selig U, Schiever U (2003) Viability of bacteria from different aquatic habitats. I. Environmental conditions and productivity. Aquat Microb Ecol 32:121–135

    Google Scholar 

  • Sedwick PN, Ditullio GR, Mackey DJ (2000) Iron and manganese in the Ross Sea: seasonal iron limitation in Antarctic shelf waters. J Geophys Res 105:11321–11336

    Article  Google Scholar 

  • Sempéré R, Van Wambeke F, Azourmanian H, Chambaut AL, Ferrière L, Bianchi M (1998) On the use of batch systems to determine DOC bacterial lability and bacterial growth efficiency in seawater samples. In: Baeyens J, Dehairs F, Goyens L (eds) Integrated marine system analysis. European Network for integrated Marine System Analysis, pp 233–238

  • Simon M, Azam F (1989) Protein content and protein synthesis rate of planktonic marine bacteria. Mar Ecol Progr Ser 51:201–213

    Google Scholar 

  • Smith EM (1998) Coherence of microbial respiration rate and cell-specific bacterial activity in a coastal planktonic community. Aquat Microb Ecol 16:27–35

    Google Scholar 

  • Smith WO Jr, Nelson DM, DiTullio GR, Leventer AR (1996) Temporal and spatial patterns in the Ross Sea: phytoplankton biomass, elemental composition, productivity and growth rates. J Geophys Res 101:18455–18466

    Article  Google Scholar 

  • Smith WO Jr, Marra J, Hiscock MR, Barber RT (2000) The seasonal cycle of phytoplankton biomass and primary productivity in the Ross sea, Antarctica. Deep-Sea Res II 47:3119–3140

    Article  Google Scholar 

  • Smith WO Jr, Dennett MR, Mathot S, Caron DA (2003) The temporal dynamics of the flagellated and colonial stages of Phaeocystis antarctica in the Ross Sea. Deep-Sea Res II 50:605–617

    Article  Google Scholar 

  • Solomon CM, Lessard EJ, Keil RG, Foy MS (2003) Characterization of extracellular polymers of Phaeocystis globosa and P. antarctica. Mar Ecol Prog Ser 250:81–89

    Google Scholar 

  • Sugimura Y, Suzuki Y (1988) A high temperature catalytic oxidation method for the determination of non-volatile dissolved organic carbon in seawater by direct injection of a liquid sample. Mar Chem 24:105–131

    Article  Google Scholar 

  • Sunda WG, Huntsman SA (1995) Iron uptake and growth limitation in oceanic and coastal phytoplankton. Mar Chem 50:189–206

    Article  Google Scholar 

  • Suzuki K, Hinuma A, Saito H, Kiyosawa H, Liu H, Saino T et al (2005) Response of phytoplankton and heterotrophic bacteria in the northwest subarctic Pacific to in situ iron fertilization as estimated by HPLC pigment analysis and flow cytometry. Prog Oceanogr. DOI: 10.1016/j.pocean.2005.02.007

  • Thingstad F, Billen G (1994) Microbial degradation of Phaeocystis material in the water column. J Mar Syst 5(1):55–65

    Article  Google Scholar 

  • Thingstad TF, Lignell R (1997) Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquat Microb Ecol 13:19–27

    Google Scholar 

  • Thingstad TF, Hagström A, Rassoulzadegan F (1997) Accumulation of degradable DOC in surface waters: is it caused by a malfunctioning microbial loop? Limnol Oceanogr 42(2):398–404

    Article  Google Scholar 

  • Tortell PD, Maldonado MT, Price NM (1996) The role of heterotrophic bacteria in the iron-limited ocean ecosystems. Nature 383:330–332

    Article  Google Scholar 

  • Tortell PD, Maldonado MT, Granger J, Price NM (1999) Marine bacteria and biogeochemical cycling of iron in the oceans. FEMS Microb Ecol 29:1–11

    Article  Google Scholar 

  • Tremblay J-E, Price NM (2002) The effect of iron in the C/N/P/Si composition of phytoplankton: does Fe-deficiency affect structural or labile, soluble pools? Ocean Sciences Meeting, Hawaii, Feb. 11–15

  • Utermölh H (1958) Zur Vervelkommnung der quantitativen Phytoplankton-Methodik. Mitt Int Verein Theor Angew Limnol 9:1–38

    Google Scholar 

  • Vaillancourt RD, Marra J, Barber RT, Smith WO Jr (2003) Primary productivity and in situ quantum yields in the Ross Sea and Pacific Sector of the Antarctic Circumpolar Current. Deep-Sea Res II 50:559–578

    Article  Google Scholar 

  • van Leeuwe MA, Stefels J (1998) Effects of iron and light stress on the biochemical composition of Antarctic Phaeocystis sp. (Prymnesiophycea). II. Pigment composition. J Phycol 34:496–503

    Article  Google Scholar 

  • Verity PG, Villareal TA, Smayda TJ (1988) Ecological investigations of blooms of colonial Phaeocystis pouchetti – 1. Abundance, biochemical composition, and metabolic rates. J Plankton Res 10(2):219–248

    Article  Google Scholar 

  • Watson SW, Novitsky TJ, Quinby HL, Valois FW (1977) Determination of bacterial number and biomass in the marine environment. Appl Environ Microbiol 33:940–946

    Google Scholar 

  • Weaver RS, Kirchman DL, Hutchins DA (2003) Utilization of iron/organic ligand complexes by marine bacterioplankton. Aquat Microb Ecol 31:227–239

    Google Scholar 

  • Weinbauer MG, Arrieta JM, Herndl GJ (2003) Stimulation of viral infection of bacterioplankton during a mesoscale iron fertilization experiment in the Southern ocean. Geophys Res abstracts 5:12280

    Google Scholar 

  • Wilcox RM, Fuhrman JA (1994) Bacterial viruses in coastal seawater: lytic rather than lysogenic production. Mar Ecol Progr Ser 114:35–45

    Google Scholar 

  • Yentsch CS, Menzel DW (1963) A method for the determination of phytoplankton chlorophyll and phaeophytin by fluorescence. Deep-Sea Res 10:221–231

    Google Scholar 

Download references

Acknowledgments

We are especially grateful to Geraldine Sarthou (LEMAR, Brest, France) for measuring Fe concentrations. We thank Natacha Brion and Nicolas Savoye for POC and PON measurements, Jeroen de Jong and Delphine Lannuzel for their help during the experiments and Elsa Breton for her help in the statistical analysis. We also thank three anonymous reviewers for their comments and suggestions, which greatly improved the manuscript. This research was supported by the Belgian Science policy (contract no. EV/11/7B—BELCANTO II) and the Belgian French Community (ARC-contract 02/07-287-SIBCLIM). This is also a contribution to the SOLAS international research initiative, the European Network of Excellence EUR-OCEANS (contract no. 511106-2).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. Becquevort.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Becquevort, S., Lancelot, C. & Schoemann, V. The role of iron in the bacterial degradation of organic matter derived from Phaeocystis antarctica . Biogeochemistry 83, 119–135 (2007). https://doi.org/10.1007/s10533-007-9079-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10533-007-9079-1

Keywords

  • Bacterioplankton
  • Iron
  • Organic matter
  • Phaeocystis antarctica
  • Remineralisation