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Environmental problems - Chemical approaches
RESEARCH ARTICLE

Carbon monoxide emissions by phytoplankton: evidence from laboratory experiments

Valérie Gros A E , Ilka Peeken B C D , Katrin Bluhm B , Eckart Zöllner B , Roland Sarda-Esteve A and Bernard Bonsang A
+ Author Affiliations
- Author Affiliations

A Laboratoire des Sciences du Climat et de l’Environnement-Unité mixte CEA-CNRS-UVSQ, F-91191 Gif sur Yvette, France.

B IFM-GEOMAR, Leibniz Institute of Marine Sciences, Marine Biogeochemistry, Westshore Building, Duesternbrooker Weg 20, D-24105 Kiel, Germany.

C Center for Marine Environmental Sciences, MARUM, Leobener Strasse, D-28359 Bremen, Germany.

D Alfred-Wegener-Institute for Polar- and Marine Research, Biological Oceanography, Am Handelshafen 12, D-27570 Bremerhaven, Germany.

E Corresponding author. Email: valerie.gros@lsce.ipsl.fr

Environmental Chemistry 6(5) 369-379 https://doi.org/10.1071/EN09020
Submitted: 13 February 2009  Accepted: 8 August 2009   Published: 22 October 2009

Environmental context. Carbon monoxide (CO) is a key component for atmospheric chemistry and its production in the ocean, although minor at the global scale, could play a significant role in the remote marine atmosphere. Up to now, CO production in the ocean was considered to mainly originate from the photo-production of dissolved organic matter (mainly under UV radiation). In this paper, we show evidence for direct production of CO by phytoplankton and we suggest it as a significant mechanism for CO production in the ocean.

Abstract. In order to investigate carbon monoxide (CO) emissions by phytoplankton organisms, a series of laboratory experiments was conducted in Kiel (Germany). Nine monocultures, including diatoms, coccolithophorids, chlorophytes and cyanobacteria have been characterised. This was done by following the CO variations from monoculture aliquots exposed to photosynthetically active radiation during one or two complete diurnal cycles. All the studied cultures have shown significant CO production when illuminated. Emission rates have been estimated to range from 1.4 × 10–5 to 8.7 × 10–4 μg of CO μg chlorophyll–1 h–1 depending on the species. When considering the magnitude of the emission rates from the largest CO emitters (cyanobacteria and diatoms), this biotic source could represent up to 20% of the CO produced in oceanic waters. As global models currently mainly consider CO production from the photo-degradation of dissolved organic matter, this study suggests that biotic CO production should also be taken into account. Whether this biological production might also contribute to some degree to the previous observed non-zero CO production below the euphotic zone (dark CO production) cannot be deduced here and needs to be further investigated.

Additional keywords: biological production, CO, ocean, monocultures.


Acknowledgements

The authors thank all the other OOMPH participants to the Kiel laboratory campaign with special thanks to Tom Custer for helping in the set-up of the analytical system. Jonathan Williams, coordinator of the OOMPH project, is gratefully acknowledged for his support during the whole project and for fruitful discussion. The authors thank Carl Brenninkmeijer and Klaus Koeppel for use of the Sofnocat. Anonymous reviewers are thanked for their comments and suggestions which helped to improve the manuscript. The Project OOMPH is funded by the European community (SUSTDEV-2004-3.I.2.1.). This is a LSCE contribution 4009.


References


[1]   J. Swinnerton , V. Linnenbo , R. Lamontagne , Ocean: a natural source of carbon monoxide. Science 1970 , 167,  984.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[2]   A. Stubbins , G. Uhera , V. Kitidis , C. S. Law , R. C. Upstill-Goddard , E. M. S. Woodward , The open-ocean source of atmospheric carbon monoxide. Deep Sea Res. Part II Top. Stud. Oceanogr. 2006 , 53,  1685.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[3]   S. P. Chu , S. Elliott , D. Erickson , Basin-scale carbon monoxide distributions in the parallel ocean program. Earth Interact. 2007 , 11,  1.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[4]   J. Swinnerton , R. Lamontagne , Carbon monoxide in South Pacific Ocean. Tellus 1974 , 26,  136.
         open url image1

[5]   R. Conrad , W. Seiler , G. Bunse , H. Giehl , Carbon-monoxide in seawater (Atlantic Ocean). Journal of Geophysical Research – Oceans 1982 , 87,  8839.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[6]   J. E. Johnson , T. S. Bates , Sources and sinks of carbon monoxide in the mixed layer of the tropical South Pacific Ocean. Global Biogeochem. Cy. 1996 , 10,  347.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[7]   D. F. Wilson , J. Swinnerton , R. Lamontagne , Production of carbon monoxide and gasesous hydrocarbons in seawater - relation to dissolved organic carbon. Science 1970 , 168,  1577.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[8]   Y. Zuo , R. D. Jones , Formation of carbon-monoxide by photolysis of dissolved marine organic material and its significance in the carbon cycling of the oceans. Naturwissenschaften 1995 , 82,  472.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[9]   O. C. Zafiriou , S. S. Andrews , W. Wang , Concordant estimates of oceanic carbon monoxide source and sink processes in the Pacific yield a balanced global ‘blue-water’ CO budget. Global Biogeochem. Cy. 2003 , 17,  1015.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[10]   R. L. Valentine , R. G. Zepp , Formation of carbon-monoxide from the photodegradation of terrestrial dissolved organic-carbon in natural-waters. Environ. Sci. Technol. 1993 , 27,  409.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[11]   Y. Zhang , H. X. Xie , G. H. Chen , Factors affecting the efficiency of carbon monoxide photoproduction in the St. Lawrence estuarine system (Canada). Environ. Sci. Technol. 2006 , 40,  7771.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[12]   L. A. Ziolkowski , W. L. Miller , Variability of the apparent quantum efficiency of CO photoproduction in the Gulf of Maine and Northwest Atlantic. Mar. Chem. 2007 , 105,  258.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[13]   H. X. Xie , S. Belanger , S. Demers , W. F. Vincent , T. N. Papakyriakou , Photobiogeochemical cycling of carbon monoxide in the southeastern Beaufort Sea in spring and autumn. Limnol. Oceanogr. 2009 , 54,  234.
         open url image1

[14]   A. J. Kettle , Comparison of dynamic models to predict the concentration of a photochemical tracer in the upper ocean as a function of depth and time. Mar. Freshwater Res. 2000 , 51,  289.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[15]   A. J. Kettle , Diurnal cycling of carbon monoxide (CO) in the upper ocean near Bermuda. Ocean Model. 2005 , 8,  337.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[16]   A. Stubbins , G. Uher , C. S. Law , K. Mopper , C. Robinson , R. C. Upstill-Goddard , Open-ocean carbon monoxide photoproduction. Deep-sea Res. Pt II 2006 , 53,  1695.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[17]   A. Stubbins , V. Hubbard , G. Uher , C. S. Law , R. C. Upstill-Goddard , G. R. Aiken , K. Mopper , Relating carbon monoxide photoproduction to dissolved organic matter functionality. Environ. Sci. Technol. 2008 , 42,  3271.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[18]   R. Conrad , W. Seiler , Photo-oxidative production and microbial consumption of carbon monoxide in seawater. FEMS Microbiol. Lett. 1980 , 9,  61.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[19]   R. F. Troxler , J. M. Dokos , Formation of carbon-monoxide and bile pigment in red and blue-green-algae. Plant Physiol. 1973 , 51,  72.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[20]   M. W. Loewus , C. C. Delwiche , Carbon monoxide production by algae. Plant Physiol. 1963 , 38,  371.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[21]   G. M. King , Aspects of carbon monoxide production and oxidation by marine macroalgae. Mar. Ecol. Prog. Ser. 2001 , 224,  69.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[22]   K. Bauer , R. Conrad , W. Seiler , Photo-oxidative production of carbon-monoxide by phototropic microorganisms. Biochim. Biophys. Acta 1980 , 589,  46.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[23]   S. L. Shaw , S. W. Chisholm , R. G. Prinn , Isoprene production by Prochlorococcus, a marine cyanobacterium, and other phytoplankton. Mar. Chem. 2003 , 80,  227.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[24]   M. D. Mackey , D. J. Mackey , H. W. Higgings , S. W. Wright , ‘CHEMTAX’ – a program for estimating class abundances from chemical markers: application to HPLC measurements of phytoplankton. Mar. Ecol. Prog. Ser. 1996 , 144,  265.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[25]   A. Colomb , N. Yassaa , J. Williams , I. Peeken , K. Lochte , Screening volatile organic compounds (VOCs) emissions from five marine phytoplankton species by head space gas chromatography/mass spectrometry (HS-GC/MS). J. Environ. Monit. 2008 , 10,  325.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[26]   R. Rippka , T. Coursin , W. Hess , C. Lichtle , D. J. Scanlan , K. A. Palinska , I. Iteman , F. Partensky , J. Houmard , M. Herdman , Prochlorococcus marinus Chisholm et al. 1992 subsp. pastoris subsp. Nov. strain PCC 9511, the first axenic chlorophyll a(2)/b(2)-containing cyanobacterium (Oxyphotobacteria). Int. J. Syst. Evol. Microbiol. 2000 , 50,  1833.
         open url image1

[27]   Y. B. Chen , J. P. Zehr , M. Mellon , Growth and nitrogen fixation of the diazotrophic filamentous nonheterocystous cyanobacterium Trichodesmium sp. IMS 101 in defined media: Evidence for a circadian rhythm. J. Phycol. 1996 , 32,  916.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[28]   Guillard R. R. L., Culture of phytoplankton for feeding marine invertebrates, in Culture of Marine Invertebrate Animals (Eds W. L. Smith, M. H. Chanley) 1975, pp. 26–60 (Plenum Press: New York).

[29]   R. R. L. Guillard , J. H. Ryther , Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea Cleve. Can. J. Microbiol. 1962 , 8,  229.
         open url image1

[30]   V. Gros , B. Bonsang , R. S. Esteve , Atmospheric carbon monoxide ‘in situ’ monitoring by automatic gas chromatography. Chemosphere, Glob. Chang. Sci. 1999 , 1,  153.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[31]   N. A. Welschmeyer , Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnol. Oceanogr. 1994 , 39,  1985.
         open url image1

[32]   Utermöhl H., Zur Vervollkommnung der quantitativen Phytoplankton Methodik 1958 (E. Schweizerbart’sche Verlagsbuchhandlung, Science Publishers: Stuttgart).

[33]   D. Marie , F. Partensky , S. Jacquet , D. Vaulot , Enumeration and cell cycle analysis of natural populations of marine picoplankton by flow cytometry usingthe nucleic acid stain SYBR Green I. Appl. Environ. Microbiol. 1997 , 63,  186.
         open url image1

[34]   H. Hillebrand , C.-D. Dürselen , D. Kirschtel , U. Pollingher , T. Zohary , Biovolume calculation for pelagic and benthic microalgae. J. Phycol. 1999 , 35,  403.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[35]   S. Menden-Deuer , E. J. Lessard , Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnol. Oceanogr. 2000 , 45,  569.
         open url image1

[36]   J. M. Gasol , P. A. Del Giorgio , Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities. Sci. Mar. 2000 , 64,  197.
         open url image1

[37]   S. Lee , J. A. Fuhrman , Relationships between biovolume and biomass of naturally derived marine bacterioplankton. Appl. Environ. Microb. 1987 , 53,  1298.
         open url image1

[38]   W. Seiler , H. Giehl , G. Bunse , Influence of plants on atmospheric carbon-monoxide and dinitrogen oxide. Pure Appl. Geophys. 1978 , 116,  439.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[39]   S. S. Wilks , Carbon monoxide in green plants. Science 1959 , 129,  964.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[40]   E. W. Chappelle , Carbon monoxide oxidation by algae. Biochim. Biophys. Acta 1962 , 62,  45.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[41]   S. W. Ragsdale , Life with carbon monoxide. Crit. Rev. Biochem. Mol. Biol. 2004 , 39,  165.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[42]   B. B. Prézelin , Diel periodicity in phytoplankton productivity. Hydrobiologia 1992 , 238,  1.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[43]   J. C. Dunlap , Molecular bases for circadian clocks. Cell 1999 , 96,  271.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[44]   H. Iwasaki , J. C. Dunlap , Microbial circadian oscillatory systems in Neurospora and Synechococcus: models for cellular clocks. Curr. Opin. Microbiol. 2000 , 3,  189.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[45]   R. F. Troxler , Synthesis of bile pigments in plants formation of carbon-monoxide and phycocyanobilin in wild-type and mutant strains of alga, Cyanidium caldarium. Biochemistry 1972 , 11,  4235.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[46]   A. Mecherikunnel , C. H. Duncan , Total and spectral solar irradiance measured at ground surface. Appl. Opt. 1982 , 21,  554.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[47]   A. D. Giles-Guzmán , S. Alvarez-Borrego , Vertical attenuation coefficient of photosynthetically active radiation as a function of chlorophyll concentration and depth in case 1 waters. Appl. Opt. 2000 , 39,  1351.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1

[48]   S. Alvain , C. Moulin , Y. Dandonneau , H. Loisel , Seasonal distribution and succession of dominant phytoplankton groups in the global ocean: A satellite view. Global Biogeochem. Cy. 2008 , 22,  GB3001.
        | Crossref | GoogleScholarGoogle Scholar |  open url image1