Evidence for marine production of monoterpenes

Noureddine Yassaa; Ilka Peeken; Eckart Zöllner; Katrin Bluhm; Steve Arnold; Dominick Spracklen; Jonathan Williams

doi:10.1071/EN08047

RESEARCH ARTICLE (Open Access)

Evidence for marine production of monoterpenes

Noureddine Yassaa ^A ^B , Ilka Peeken ^C ^D , Eckart Zöllner ^C , Katrin Bluhm ^C , Steve Arnold ^E , Dominick Spracklen ^E and Jonathan Williams ^A ^F

+ Author Affiliations

- Author Affiliations

^A Air Chemistry Department, Max Planck Institute for Chemistry, D-55020 Mainz, Germany.

^B Faculty of Chemistry, University of Sciences and Technology Houari Boumediene (U.S.T.H.B.), Bab-Ezzouar, 16111 Algiers, Algeria.

^C Leibniz Institute of Marine Sciences at the University of Kiel (IFM GEOMAR), Biological Oceanography, D-24105 Kiel, Germany.

^D Present address: Center for Marine Environmental Sciences MARUM, Bremen, Germany, and Alfred Wegener Institute of Polar and Marine Research, D-27570 Bremerhaven, Germany.

^E Institute for Climate and Atmospheric Science, Environment Building, School of Earth and Environment, University of Leeds, Leeds, LS2 9JT, United Kingdom.

^F Corresponding author. Email: williams@mpch-mainz.mpg.de

Environmental Chemistry 5(6) 391-401 https://doi.org/10.1071/EN08047
Submitted: 7 August 2008 Accepted: 5 November 2008 Published: 18 December 2008

Environmental context. Laboratory incubation experiments and shipboard measurements in the Southern Atlantic Ocean have provided the first evidence for marine production of monoterpenes. Nine marine phytoplankton monocultures were investigated using a GC-MS equipped with an enantiomerically-selective column and found to emit monoterpenes including (–)-/(+)-pinene, limonene and p-ocimene, all of which were previously thought to be exclusively of terrestrial origin. Maximum levels of 100–200 pptv total monoterpenes were encountered when the ship crossed an active phytoplankton bloom.

Abstract. Laboratory incubation experiments and shipboard measurements on the Southern Atlantic Ocean have provided the first evidence for marine production of monoterpenes. Nine marine phytoplankton monocultures were investigated using a GC-MS equipped with an enantiomerically-selective column and found to emit at rates, expressed as nmol C₁₀H₁₆ (monoterpene) g [chlorophyll a]^–1 day^–1, from 0.3 nmol g [chlorophyll a]^–1 day^–1 for Skeletonema costatum and Emiliania huxleyi to 225.9 nmol g [chlorophyll a]^–1 day^–1 for Dunaliella tertiolecta. Nine monoterpenes were identified in the sample and not in the control, namely: (–)-/(+)-pinene, myrcene, (+)-camphene, (–)-sabinene, (+)-3-carene, (–)-pinene, (–)-limonene and p-ocimene. In addition, shipboard measurements of monoterpenes in air were made in January–March 2007, over the South Atlantic Ocean. Monoterpenes were detected in marine air sufficiently far from land as to exclude influence from terrestrial sources. Maximum levels of 100–200 pptv total monoterpenes were encountered when the ship crossed an active phytoplankton bloom, whereas in low chlorophyll regions monoterpenes were mostly below detection limit.

Additional keywords: algae, isoprene, organic trace gases, Southern Atlantic Ocean.

Acknowledgements

This work was completed as part of the OOMPH project (Specific Targeted Research Project (STREP) in the Global Change and Ecosystems Sub-Priority). SUSTDEV-2004-3.I.2.1. Project Number 018419. The authors are grateful for logistical support from the IPEV/Aerotrace program during the Southern Ocean cruise. The authors thank Tom Custer for his technical assistance during the laboratory experiments and the cruise and for making the back-trajectory figures, and Rolf Hofmann, Thomas Küpfel, Sarah Gebhardt, Vinayak Sinha and Aurélie Colomb for their technical assistance during the cruise.

References

[1] J. Williams , Organic trace gases in the atmosphere: an overview. Environ. Chem. 2004 , 1, 125.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[2] A. Guenther , C. N. Hewitt , D. Erickson , R. Fall , C. Geron , T. Graedel , P. Harley , L. Klinger , et al. A global-model of natural volatile organic compound emissions. J. Geophys. Res. 1995 , 100, 8873.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[3] Atlas E. L. S., Li S. M., Standley L. J., Hites R. A., in Global Atmospheric Change (Eds C. N. Hewitt, W. T. Sturges) 1994, pp. 313–381 (Chaman and Hall: London).

[4] Ciccioli P., Brancaleoni E., Frattoni M., in Reactive Hydrocarbons in the Atmosphere (Ed. C. N. Hewitt) 1999, pp. 159–207 (Academic Press: New York).

[5] C. Plass-Dülmer , R. Koppmann , M. Ratte , J. Rudolph , Light nonmethane hydrocarbons in seawater. Global Biogeochem. Cy. 1995 , 9, 79.
        | Crossref | GoogleScholarGoogle Scholar |

[6] H. B. Singh , A. Tabazadeh , M. J. Evans , B. D. Field , D. J. Jacob , G. Sachse , J. H. Crawford , R. Shetter , W. H. Brune , Oxygenated volatile organic chemicals in the oceans: interferences and implications based on atmospheric observations and air–sea flux exchange models. Geophys. Res. Lett. 2003 , 30, 1862.
        | Crossref | GoogleScholarGoogle Scholar |

[7] C. D. O’Dowd , M. C. Facchini , F. Cavalli , D. Ceburnis , M. Mircea , S. Decesari , S. Fuzzi , Y. J. Yoon , J. P. Putaud , Biogenically driven organic contribution to marine aerosol. Nature 2004 , 431, 676.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[8] Keller M. D., Bellows W. K., Guillard R. R. L., in Biogenic Sulfur in the Environment (Eds E. S. Saltzmann, W. J. Cooper) 1989, pp. 167–182 (American Chemical Society: Washington, DC).

[9] P. S. Liss , A. D. Hatton , G. Malin , P. D. Nightingale , S. M. Turner , Marine sulphur emissions. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1997 , 352, 159.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[10] R. P. Kiene , T. S. Bates , Biological removal of dimethyl sulphide from seawater. Nature 1990 , 345, 702.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[11] R. P. Kiene , L. J. Linn , J. A. Bruton , New and important roles for DMSP in marine microbial communities. J. Sea Res. 2000 , 43, 209.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[12] B. Bonsang , C. Polle , G. Lambert , Evidence for marine production of isoprene. Geophys. Res. Lett. 1992 , 19, 1129.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[13] W. J. Broadgate , P. S. Liss , S. A. Penkett , Seasonal emissions of isoprene and other reactive hydrocarbon gases from the ocean. Geophys. Res. Lett. 1997 , 24, 2675.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[14] W. J. Broadgate , G. Malin , F. C. Kupper , A. Thompson , P. S. Liss , Isoprene and other non-methane hydrocarbons from seaweeds: a source of reactive hydrocarbons to the atmosphere. Mar. Chem. 2004 , 88, 61.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[15] P. J. Milne , D. D. Riemer , R. G. Zika , L. E. Brand , Measurement of vertical-distribution of isoprene in surface seawater, its chemical fate, and its emission from several phytoplankton monocultures. Mar. Chem. 1995 , 48, 237.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[16] R. M. Moore , D. E. Oram , S. A. Penkett , Production of isoprene by marine-phytoplankton cultures. Geophys. Res. Lett. 1994 , 21, 2507.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[17] 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 | CAS |

[18] M. Claeys , B. Graham , G. Vas , W. Wang , R. Vermeylen , V. Pashynska , J. Cafmeyer , P. Guyon , M. O. Andreae , P. Artaxo , W. Maenhaut , Formation of secondary organic aerosols through photooxidation of isoprene. Science 2004 , 303, 1173.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[19] N. Meskhidze , A. Nenes , Phytoplankton and cloudiness over the Southern Ocean. Science 2006 , 314, 1419.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[20] J. H. Seinfeld , J. F. Pankow , Organic atmospheric particulate material. Annu. Rev. Phys. Chem. 2003 , 54, 121.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[21] M. Jaoui , R. M. Kamens , Mass balance of gaseous and particulate products from beta-pinene/O₃/air in the absence of light and beta-pinene/NO_x/air in the presence of natural sunlight. J. Atmos. Chem. 2003 , 45, 101.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[22] J. H. Kroll , Secondary organic aerosol formation from isoprene phtooxidation. Environ. Sci. Technol. 2006 , 40, 1869.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[23] R. Croteau , Biosynthesis and catabolism of monoterpenoids. Chem. Rev. 1987 , 87, 929.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[24] Lough W. J., Wainer I. W. (Eds), Chirality in Natural and Applied Science 2002 (Blackwell Publishing: Oxford, UK).

[25] 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 a₂/b₂-containing cyanobacterium (Oxyphotobacteria). Int. J. Syst. Evol. Microbiol. 2000 , 50, 1833.
        | CAS | PubMed |

[26] 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 |

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

[28] 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.
        | CAS | PubMed |

[29] L. Hoffmann , I. Peeken , K. Lochte , P. Assmy , M. Veldhuis , Different reactions of Southern Ocean phytoplankton size classes to iron fertilization. Limnol. Oceanogr. 2006 , 51, 1217.
        | CAS |

[30] 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 | CAS |

[31] M. J. W. Veldhuis , G. W. Kraay , Phytoplankton in the subtropical Atlantic Ocean; towards a better understanding of biomass and composition. Deep-Sea Res. 2004 , I51, 507.


[32] Methven J., Offline trajectories: Calculation and accuracy, Tech. Rep. 44, UK University Global Atmospheric Modelling Programme, Department of Meteorology 1997 (University of Reading: Reading, UK).

[33] N. Yassaa , J. Williams , Analysis of enantiomeric and non-enantiomeric monoterpenes in plant emissions using portable dynamic air sampling/solid-phase microextraction (PDAS-SPME) and chiral gas chromatography/mass spectrometry. Atmos. Environ. 2005 , 39, 4875.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[34] J. Williams , N. Yassaa , S. Bartenbach , J. Lelieveld , Mirror image hydrocarbons from Tropical and Boreal forests. Atmos. Chem. Phys. 2007 , 7, 973.
        | CAS |

[35] M. L. Wise , G. L. Rorrer , J. J. Polzin , R. Croteau , Biosynthesis of marine natural products: isolation and characterization of a myrcene synthase from cultured tissues of the marine red alga Ochtodes secundiramea. Arch. Biochem. Biophys. 2002 , 400, 125.
        | Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

[36] M. L. Wise , Monoterpene biosynthesis in marine algae. Phycologia 2003 , 42, 370.


[37] J. M. Hunt , R. J. Miller , J. K. Whelan , Formation of C4–C7 hydrocarbons from bacterial degradation of naturally occurring terpenoids. Nature 1980 , 288, 577.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

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

[39] A. C. Lewis , L. J. Carpenter , M. J. Pilling , Nonmethane hydrocarbons in Southern Ocean boundary layer air. J. Geophys. Res. – Atmos 2001 , 106, 4987.
        | Crossref | GoogleScholarGoogle Scholar | CAS |

[40] P. I. Palmer , S. L. Shaw , Quantifying global marine isoprene fluxes using MODIS chlorophyll observations. Geophys. Res. Lett. 2005 , 32, L09805.
        | Crossref | GoogleScholarGoogle Scholar |

[41] J. Williams , U. Pöschl , P. J. Crutzen , A. Hansel , R. Holzinger , C. Warneke , W. Lindinger , J. Lelieveld , An atmospheric chemistry interpretation of mass scans obtained from a Proton Transfer Mass spectrometer flown over the tropical rainforest of Surinam. J. Atmos. Chem. 2001 , 38, 133.
        | Crossref | GoogleScholarGoogle Scholar | CAS |