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RESEARCH ARTICLE

Influence of culture regime on arsenic cycling by the marine phytoplankton Dunaliella tertiolecta and Thalassiosira pseudonana

Elliott G. Duncan A B , William A. Maher A , Simon D. Foster A and Frank Krikowa A
+ Author Affiliations
- Author Affiliations

A Ecochemistry Laboratory, Institute for Applied Ecology, University of Canberra, University Drive, Bruce, ACT 2601, Australia.

B Corresponding author. Email: elliott.duncan@canberra.edu.au

Environmental Chemistry 10(2) 91-101 https://doi.org/10.1071/EN12191
Submitted: 6 December 2012  Accepted: 9 February 2013   Published: 18 April 2013

Environmental context. Phytoplankton form the base of marine food-webs, and hence they have been proposed as the likely source of many arsenic compounds found in marine animals. Because of the difficulties associated with field experiments with phytoplankton, attempts to test this hypothesis have relied mainly on laboratory experiments. This study assesses the environmental validity of this research approach by investigating the influence of the culturing experimental protocol on the uptake, accumulation and biotransformation of arsenic by marine phytoplankton.

Abstract. Arsenic cycling by the marine phytoplankton Dunaliella tertiolecta and the marine diatom Thalassiosira pseudonana was influenced by culture regime. Arsenic was associated with the residue cell fractions of batch cultured phytoplankton (D. tertiolecta and T. pseudonana), due to the accumulation of dead cells within batch cultures. Greater arsenic concentrations were associated with water-soluble and lipid-soluble cell fractions of continuously cultured phytoplankton. Arsenoribosides (as glycerol (Gly-), phosphate (PO4-) and sulfate (OSO3-)) were ubiquitous in D. tertiolecta (Gly- and PO4- only) and T. pseudonana (all three species). Additionally, arsenobetaine (AB) was not detected in any phytoplankton tissues, illustrating that marine phytoplankton themselves are not an alternate source of AB. Arsenic species formation was influenced by culture regime, with PO4-riboside produced under nutrient rich conditions, whereas Dimethylarsenoacetate (DMAA) was found in old (>42 days old) batch cultures, with this arsenic species possibly produced by the degradation of arsenoribosides-arsenolipids from decomposing cells rather than by biosynthesis. Nutrient availability, hence culture regime was thus influential in directly and indirectly influencing arsenic cycling and the arsenic species produced by D. tertiolecta and T. pseudonana. Future research should thus utilise continuous culture regimes to study arsenic cycling as these are far more analogous to environmental processes.

Additional keywords: arsenic species, arsenoribosides, batch culture, continuous culture, lipid-soluble arsenic.


References

[1]  C. Humborg, D. J. Conley, L. Rahm, F. Wulff, A. Cociasu, V. Ittekkot, Silicon retention in river basins: far-reaching effects on biogeochemistry and aquatic food webs in coastal marine environments. Ambio 2000, 29, 45.

[2]  J. S. Edmonds, Y. Shibata, K. A. Francesconi, R. J. Rippington, M. Morita, Arsenic transformations in short marine food chains studies by HPLC-ICP MS. Appl. Organomet. Chem. 1997, 11, 281.
Arsenic transformations in short marine food chains studies by HPLC-ICP MS.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXis12qsr8%3D&md5=e594f9d26aae431e337a7a11bb5c71dcCAS |

[3]  W. Maher, S. Foster, F. Krikowa, Arsenic species in Australian temperate marine food chains. Mar. Freshwater Res. 2009, 60, 885.
Arsenic species in Australian temperate marine food chains.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFGhs77F&md5=2fb12e90533d4a845bb4da9dca903051CAS |

[4]  J. G. Sanders, R. W. Osman, G. F. Reidel, Pathways of arsenic uptake and incorporation in estuarine phytoplankton and the filterfeeding invertebrates Eurytemora affinis, Balanus improvisus and Crassostrea virginica. Mar. Biol. 1989, 103, 319.
Pathways of arsenic uptake and incorporation in estuarine phytoplankton and the filterfeeding invertebrates Eurytemora affinis, Balanus improvisus and Crassostrea virginica.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXnsVaisA%3D%3D&md5=2e42732683a3575f074049c02ab807a8CAS |

[5]  E. Duncan, S. Foster, W. Maher, Uptake and metabolism of arsenate, methylarsonate and arsenobetaine by axenic cultures of the phytoplankton Dunaliella tertiolecta. Bot. Mar. 2010, 53, 377.
Uptake and metabolism of arsenate, methylarsonate and arsenobetaine by axenic cultures of the phytoplankton Dunaliella tertiolecta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlKis7bI&md5=7640b9cd642361413ab7159a54256d0dCAS |

[6]  S. Foster, D. Thomson, W. Maher, Uptake and metabolism of arsenate by anexic cultures of the microalgae Dunaliella tertiolecta and Phaeodactylum tricornutum. Mar. Chem. 2008, 108, 172.
Uptake and metabolism of arsenate by anexic cultures of the microalgae Dunaliella tertiolecta and Phaeodactylum tricornutum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnvVyrtQ%3D%3D&md5=6284ad256918bfe236639a76386bfb1bCAS |

[7]  W. R. Cullen, L. G. Harrison, H. Li, G. Hewitt, Bioaccumulation and excretion of arsenic compounds by a marine unicellular alga, Polyphysa peniculus. Appl. Organomet. Chem. 1994, 8, 313.
Bioaccumulation and excretion of arsenic compounds by a marine unicellular alga, Polyphysa peniculus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXlslCru7Y%3D&md5=c4364c4061537a357d9337a7a779027eCAS |

[8]  Y. Yamaoka, O. Takimura, H. Fuse, K. Murakami, Effect of glutathione on arsenic accumulation by Dunaliella salina. Appl. Organomet. Chem. 1999, 13, 89.
Effect of glutathione on arsenic accumulation by Dunaliella salina.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhsF2gs7o%3D&md5=a7857034af24c586a2ff55508b8b4ff2CAS |

[9]  O. Takimura, H. Fuse, K. Murakami, K. Kamimura, Y. Yamaoka, Uptake and reduction of arsenate by Dunaliella sp. Appl. Organomet. Chem. 1996, 10, 753.
Uptake and reduction of arsenate by Dunaliella sp.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XnsFymsr0%3D&md5=528f4912ffcbaabf4dfa95386422817eCAS |

[10]  Y. Yamaoka, O. Takimura, H. Fuse, K. Kamimura, Accumulation of arsenic and selenium by Dunaliella sp. Appl. Organomet. Chem. 1990, 4, 261.
Accumulation of arsenic and selenium by Dunaliella sp.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXjslCiuw%3D%3D&md5=ac6e2d78cc730de7c8276dbd97236689CAS |

[11]  D. Tilman, S. S. Kilham, Phosphate and silicate growth and uptake kinetics of the diatoms Asterionella formosa and Cyclotella meneghiniana in batch and semicontinuous culture. Phycology. 1976, 12, 375.
| 1:CAS:528:DyaE2sXmvVWltg%3D%3D&md5=b8a972ee981400683c87c227875ecdb7CAS |

[12]  I. Aoyama, H. Okamura, Interactive toxic effect and bioconcentration between cadmium and chromium using continuous algal culture. Environ. Toxicol. Water Qual. 1993, 8, 255.
Interactive toxic effect and bioconcentration between cadmium and chromium using continuous algal culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlslGmtLk%3D&md5=445eb3180d6f4a1044dc4b232b4b9b5eCAS |

[13]  K. R. Arrigo, Marine microorganisms and global nutrient cycles. Nature 2005, 437, 349.
Marine microorganisms and global nutrient cycles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpvFOrtLk%3D&md5=90cda4d66ae691d11d51ee0d1161a802CAS | 16163345PubMed |

[14]  M. R. Droop, The nutrient status of algal cells in continuous culture. J. Mar. Biol. Assoc. U.K. 1974, 54, 825.
The nutrient status of algal cells in continuous culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXhtlGmsLk%3D&md5=4e8a159c5f359759619a9f0d92ebae8cCAS |

[15]  P. Sorgeloos, E. Van Outryve, G. Persoone, A. Cattoir-Reynaerts, New type of turbidostat with intermittent determination of cell density outside the culture vessel. Appl. Environ. Microbiol. 1976, 31, 327.
| 1:STN:280:DC%2BC3crnvVKrsw%3D%3D&md5=69ccafe97a181dd64aaa07d495f4e522CAS | 16345153PubMed |

[16]  E. Paasche, Silicon and the ecology of marine plankton diatoms. I. Thalassiosira pseudonana (Cyclotella nana) grown in a chemostat with silicate as limiting nutrient. Mar. Biol. 1973, 19, 117.
Silicon and the ecology of marine plankton diatoms. I. Thalassiosira pseudonana (Cyclotella nana) grown in a chemostat with silicate as limiting nutrient.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3sXkvV2gur0%3D&md5=4a788c70e4e89cc7bd9409f94a0b7c47CAS |

[17]  O. S. Okay, A. Gaines, A. M. Davie, The Growth of continuous cultures of the phytoplankton Phaeodactylum tricornutum. Turk. J. Eng. Environ. Sci. 2003, 27, 145.
| 1:CAS:528:DC%2BD3sXltV2gtL8%3D&md5=fc16c039f8b004a68b235c6b8a88908dCAS |

[18]  P. J. Harrison, H. L. Conway, R. C. Dugdale, Marine diatoms grown in chemostats under silicate or ammonium limitation. I. Cellular chemical composition and steady-state growth kinetics of Skeletonema costatum. Mar. Biol. 1976, 35, 177.
Marine diatoms grown in chemostats under silicate or ammonium limitation. I. Cellular chemical composition and steady-state growth kinetics of Skeletonema costatum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XktVagtro%3D&md5=452be2a131f508f449d4f7d080af60c8CAS |

[19]  M. J. Perry, Phosphate utilization by an oceanic diatom in phosphorus-limited chemostat culture and in the oligotrophic waters of the central North Pacific. Limnol. Oceanogr. 1976, 21, 88.
Phosphate utilization by an oceanic diatom in phosphorus-limited chemostat culture and in the oligotrophic waters of the central North Pacific.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28Xhtlamsr4%3D&md5=d09fdf22401e691e2a1d071d5f502f33CAS |

[20]  R. R. L. Guillard, J. H. Ryther, Studies on planktonic diatoms. I. Cyclotela nana (Hustedt) and Detonula confervacea (CleveGran.). Can. J. Microbiol. 1962, 8, 229.
Studies on planktonic diatoms. I. Cyclotela nana (Hustedt) and Detonula confervacea (CleveGran.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF38XktlWqu70%3D&md5=e2f28dc1b32360aa5e62a2bd4cecc394CAS |

[21]  J. L. Levy, J. L. Stauber, S. A. Wakelin, D. F. Jolley, The effect of bacteria on the sensitivity of microalgae to copper in laboratory bioassays. Chemosphere 2009, 74, 1266.
The effect of bacteria on the sensitivity of microalgae to copper in laboratory bioassays.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXitVygtr8%3D&md5=bf0c783b7ddc5a05bcc691cfb5c390eeCAS | 19101014PubMed |

[22]  S. Baldwin, M. Deaker, W. Maher, Low volume microwave digestion of marine biological tissues for the measurement of trace elements. Analyst 1994, 119, 1701.
Low volume microwave digestion of marine biological tissues for the measurement of trace elements.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmtVSgtLo%3D&md5=98c4dedcd67858998b9a2ca42de688eaCAS | 7978323PubMed |

[23]  W. Maher, S. Foster, F. Krikowa, P. Snitch, G. Chapple, P. Craig, Measurement of trace metals and phosphorus in marine animal and plant tissues by low volume microwave digestion and ICPMS. J. Anal. At. Spectrom. 2001, 22, 361.
| 1:CAS:528:DC%2BD3MXovVOisbs%3D&md5=3a52ab8bfeec6acd477a6eee744767b6CAS |

[24]  W. Maher, F. Krikowa, D. Wruck, H. Louie, T. Nguyen, W. Y. Huang, Determination of total phosphorus and nitrogen in turbid waters by oxidation with alkaline potassium peroxodisulfate and low pressure microwave digestion, autoclave heating or the use of closed vessels in a hot water bath: comparison with Kjeldahl digestion. Anal. Chim. Acta 2002, 463, 283.
Determination of total phosphorus and nitrogen in turbid waters by oxidation with alkaline potassium peroxodisulfate and low pressure microwave digestion, autoclave heating or the use of closed vessels in a hot water bath: comparison with Kjeldahl digestion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkvFGksbk%3D&md5=7efab8b7fecbd3a65c3aeec54b9e7bb9CAS |

[25]  J. Folch, M. Lees, G. H. Sloane Stanley, A simple method for the isolation and purification of total lipids from animal tissue. J. Biol. Chem. 1957, 226, 497.
| 1:STN:280:DyaG2s%2FnsFCjtw%3D%3D&md5=3360c7c6dbb3685b46b551b68d67e31cCAS | 13428781PubMed |

[26]  S. Foster, W. Maher, F. Krikowa, S. Apte, A microwave assisted sequential extraction of water and dilute acid soluble arsenic species from marine plant and animal tissues. Talanta 2007, 71, 537.
A microwave assisted sequential extraction of water and dilute acid soluble arsenic species from marine plant and animal tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXotFSltA%3D%3D&md5=ad3bb509b7834f1a0f1c878f060cec1dCAS | 19071338PubMed |

[27]  M. Deaker, W. Maher, Determination of arsenic in arsenic compounds and marine biological tissues using low volume microwave digestion and electrothermal atomic absorption spectrometry. J. Anal. At. Spectrom. 1999, 14, 1193.
Determination of arsenic in arsenic compounds and marine biological tissues using low volume microwave digestion and electrothermal atomic absorption spectrometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXltFWgt7k%3D&md5=5a01a3184252215de081c0688b965ba7CAS |

[28]  S. Foster, W. Maher, F. Krikowa, Changes in proportions of arsenic species within an Ecklonia radiata food chain. Environ. Chem. 2008, 5, 176.
Changes in proportions of arsenic species within an Ecklonia radiata food chain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntlCrtrk%3D&md5=bf4fd9e08a6482228f5213dd9c61fe10CAS |

[29]  J. Kirby, W. Maher, M. Ellwood, F. Krikowa, Arsenic species determination in biological tissues by HPLC-ICP-MS and HPLC-HG-ICP-MS. Aust. J. Chem. 2004, 57, 957.
Arsenic species determination in biological tissues by HPLC-ICP-MS and HPLC-HG-ICP-MS.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXps1SjsrY%3D&md5=8cd9c006fa35e05d1fec7b52a3033869CAS |

[30]  A. D. Madsen, W. Goessler, S. N. Pedersen, K. A. Francesconi, Characterization of an algal extract by HPLC-ICP-MS and LC-electrospray MS for use in arsenosugar speciation studies. J. Anal. At. Spectrom. 2000, 15, 657.
Characterization of an algal extract by HPLC-ICP-MS and LC-electrospray MS for use in arsenosugar speciation studies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjslWksLY%3D&md5=75e25a256d04b6a251bc93938cea9b00CAS |

[31]  J. Cannon, J. Edmonds, K. Francesconi, C. Raston, J. Saunders, B. Skelton, A. White, Isolation, crystal structure and synthesis of arsenobetaine, a constituent of the western rock lobster, the dusky shark, and some samples of human urine. Aust. J. Chem. 1981, 34, 787.
Isolation, crystal structure and synthesis of arsenobetaine, a constituent of the western rock lobster, the dusky shark, and some samples of human urine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXltFemt7k%3D&md5=2d255cb912cf5cd3bdce3d985c039460CAS |

[32]  R. Minhas, D. S. Forsyth, B. Dawson, Synthesis and characterization of arsenobetaine and arsenocholine derivatives. Appl. Organomet. Chem. 1998, 12, 635.
Synthesis and characterization of arsenobetaine and arsenocholine derivatives.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlsFOnu78%3D&md5=6dda9a12a6d6872e0cb8c199a636ecd4CAS |

[33]  G. M. Momplaisir, J. S. Blais, M. Quinteiro, W. D. Marshall, Determination of arsenobetaine, arsenocholine, and tetramethylarsonium cations in seafoods and human urine by high-performance liquid chromatography-thermochemical hydride generation-atomic absorption spectrometry. J. Agric. Food Chem. 1991, 39, 1448.
Determination of arsenobetaine, arsenocholine, and tetramethylarsonium cations in seafoods and human urine by high-performance liquid chromatography-thermochemical hydride generation-atomic absorption spectrometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXkvFSktLw%3D&md5=38c43e488e695d0bdc6dd68c37849832CAS |

[34]  A. Merijanian, R. A. Zingaro, Arsine oxides. Inorg. Chem. 1966, 5, 187.
Arsine oxides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF28Xktl2lsQ%3D%3D&md5=ddde05d777ce3ec5a07a8acec9484416CAS |

[35]  J. S. Edmonds, K. A. Francesconi, J. A. Hansen, Dimethyloxarsylethanol from anaerobic decomposition of brown kelp (Ecklonia radiata): a likely precursor of arsenobetaine in marine fauna. Experientia 1982, 38, 643.
Dimethyloxarsylethanol from anaerobic decomposition of brown kelp (Ecklonia radiata): a likely precursor of arsenobetaine in marine fauna.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38Xks12js7s%3D&md5=b70bf0b13668bddd47deb10a9341acfdCAS |

[36]  K. A. Francesconi, J. S. Edmonds, R. V. Stick, Accumulation of arsenic in yelloweye mullet (Aldrichetta forsteri) following oral administration of organoarsenic compounds and arsenate. Sci. Total Environ. 1989, 79, 59.
Accumulation of arsenic in yelloweye mullet (Aldrichetta forsteri) following oral administration of organoarsenic compounds and arsenate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXhsV2gs70%3D&md5=6124fe2f47af6b1ce2146e458c3b6801CAS | 2928771PubMed |

[37]  R. Raml, W. Goessler, K. A. Francesconi, Improved chromatographic separation of thio-arsenic compounds by reversed-phase high performance liquid chromatography–inductively coupled plasma mass spectrometry. J. Chromatogr. A 2006, 1128, 164.
Improved chromatographic separation of thio-arsenic compounds by reversed-phase high performance liquid chromatography–inductively coupled plasma mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XptFSrsr0%3D&md5=11eb5d89208df17af8b9f923f75f4208CAS | 16854422PubMed |

[38]  M. R. Droop, The nutrient status of algal cells in batch culture. J. Mar. Biol. Assoc. U.K. 1975, 55, 541.
The nutrient status of algal cells in batch culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXlvFSnsbk%3D&md5=88321fbd3740481de417b617cd658fdcCAS |

[39]  J. B. Cotner, R. G. Wetzel, Uptake of dissolved inorganic and organic phosphorus compounds by phytoplankton and bacterioplankton. Limnol. Oceanogr. 1992, 37, 232.
Uptake of dissolved inorganic and organic phosphorus compounds by phytoplankton and bacterioplankton.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XlsFOitbs%3D&md5=5ced7939155e1788057750bf0332202cCAS |

[40]  S. Maeda, K. Mawatari, A. Ohki, K. Naka, Arsenic metabolism in a freshwater food chain: blue-green alga (Nostoc sp.)+ shrimp (Neocaridina denticulata)+ carp (Cyprinus carpio). Appl. Organomet. Chem. 1993, 7, 467.
Arsenic metabolism in a freshwater food chain: blue-green alga (Nostoc sp.)+ shrimp (Neocaridina denticulata)+ carp (Cyprinus carpio).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXht12qsbw%3D&md5=3a8f8168d91c7563a2b572d6d38ec86dCAS |

[41]  S. Maeda, A. Ohki, K. Kusadome, T. Kuroiwa, L. Yoshifuku, K. Naka, Bioaccumulation of arsenic and its fate in a freshwater food chain. Appl. Organomet. Chem. 1992, 6, 213.
Bioaccumulation of arsenic and its fate in a freshwater food chain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xis1ajurc%3D&md5=7df49ab51056aebbe297577614df4496CAS |

[42]  R. S. Oremland, J. F. Stolz, The ecology of arsenic. Science 2003, 300, 939.
The ecology of arsenic.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjsVyjsLs%3D&md5=0d9d9b04d95aa8ab4cf87da7f8332cc8CAS | 12738852PubMed |

[43]  F. Hellweger, K. J. Farley, U. Lall, D. M. Di Toro, Greedy algae reduce arsenate. Limnol. Oceanogr. 2003, 48, 2275.
| 1:CAS:528:DC%2BD3sXpvFagtrY%3D&md5=eae683de18095cf985df145c84fb0937CAS |

[44]  S. García-Salgado, G. Raber, R. Raml, C. Magnes, K. A. Francesconi, Arsenosugar phospholipids and arsenic hydrocarbons in two species of brown macroalgae. Environ. Chem. 2012, 9, 63.
Arsenosugar phospholipids and arsenic hydrocarbons in two species of brown macroalgae.Crossref | GoogleScholarGoogle Scholar |

[45]  M. Suzumura, Phospholipids in marine environments: a review. Talanta 2005, 66, 422.
Phospholipids in marine environments: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjvVClt7g%3D&md5=441b5704074f5859a616c5ca02ae5dbfCAS | 18970003PubMed |

[46]  A. Hosseini Tafreshi, M. Shariati, Dunaliella biotechnology: methods and applications. J. Appl. Microbiol. 2009, 107, 14.
Dunaliella biotechnology: methods and applications.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MrisFGitA%3D%3D&md5=e468e7d5228245cbd8eb91bcdd319891CAS | 19245408PubMed |

[47]  A. Goyal, Osmoregulation in Dunaliella, part II: photosynthesis and starch contribute carbon for glycerol synthesis during a salt stress in Dunaliella tertiolecta. Plant Physiol. Biochem. 2007, 45, 705.
Osmoregulation in Dunaliella, part II: photosynthesis and starch contribute carbon for glycerol synthesis during a salt stress in Dunaliella tertiolecta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVOgurrM&md5=9773c7a8ad69292ef383e7f3dc76b90dCAS | 17764963PubMed |

[48]  J. E. Cloern, Phytoplankton bloom dynamics in coastal ecosystems: A rewiev with some general lessons from sustained investigation of San Francisco Bay, California. Rev. Geophys. 1996, 34, 127.
Phytoplankton bloom dynamics in coastal ecosystems: A rewiev with some general lessons from sustained investigation of San Francisco Bay, California.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmsVCqtLY%3D&md5=0e07aa2c2adee39c0c735ae3e5ed6ee1CAS |

[49]  S. V. Smith, Phosphorus versus nitrogen limitation in the marine environment. Limnol. Oceanogr. 1984, 29, 1149.
Phosphorus versus nitrogen limitation in the marine environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXhtVSgsbc%3D&md5=28ad6d07e05ee346f7fa29b97e55fb1eCAS |

[50]  P. R. Jensen, C. A. Kauffman, W. Fenical, High recovery of culturable bacteria from the surfaces of marine algae. Mar. Biol. 1996, 126, 1.
High recovery of culturable bacteria from the surfaces of marine algae.Crossref | GoogleScholarGoogle Scholar |

[51]  J. S. Edmonds, K. A. Francesconi, Organoarsenic compounds in the marine environment, in Organometallic Compounds in the Environment (Ed. P. J. Craig) 2003, pp. 196–222 (Wiley: New York).

[52]  F. Challenger, Biological methylation. Chem. Rev. 1945, 36, 315.
Biological methylation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaH2MXisFGrtQ%3D%3D&md5=39233cb1444b56445024781cd1919320CAS |

[53]  S. Foster, W. Maher, Degradation of arsenoribosides from marine macroalgae in simulated rock pools, in Arsenic in Geosphere and Human Diseases (Eds J. S. Jean, J. Bundschuh, P. Battacharya) 2010, pp. 230–232 (CRC Press: London).

[54]  J. Navratilova, G. Raber, S. J. Fisher, K. A. Francesconi, Arsenic cycling in marine systems: degradation of arsenosugars to arsenate in decomposing algae, and preliminary evidence for the formation of recalcitrant arsenic. Environ. Chem. 2011, 8, 44.
Arsenic cycling in marine systems: degradation of arsenosugars to arsenate in decomposing algae, and preliminary evidence for the formation of recalcitrant arsenic.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjs1GlsLc%3D&md5=44904d3f79b7ac8d228e4f6c32b6cc6dCAS |

[55]  P. Pengprecha, M. Wilson, A. Raab, J. Feldmann, Biodegradation of arsenosugars in marine sediment. Appl. Organomet. Chem. 2005, 19, 819.
Biodegradation of arsenosugars in marine sediment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtFKku70%3D&md5=cabcd88a070e0d77870de7bed693dcfdCAS |

[56]  J. Kirby, W. Maher, D. Spooner, Arsenic occurence and species in near-shore macroalgae-feeding marine animals. Environ. Sci. Technol. 2005, 39, 5999.
Arsenic occurence and species in near-shore macroalgae-feeding marine animals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtVWit7g%3D&md5=b16ba362b732e4d5d27d091c4df49e11CAS | 16173556PubMed |

[57]  J. Kirby, W. Maher, Measurement of water-soluble arsenic species in freeze-dried marine animal tissues by microwave-assisted extraction and HPLC-ICP-MS. J. Anal. At. Spectrom. 2002, 17, 838.
Measurement of water-soluble arsenic species in freeze-dried marine animal tissues by microwave-assisted extraction and HPLC-ICP-MS.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlvVKhsbs%3D&md5=78d9570cd41f9e9c2eb04d6e1da341c7CAS |

[58]  R. Tukai, W. A. Maher, I. J. McNaught, M. J. Ellwood, M. Coleman, Occurrence and chemical form of arsenic in marine macroalgae from the east coast of Australia. Mar. Freshwater Res. 2002, 53, 971.
Occurrence and chemical form of arsenic in marine macroalgae from the east coast of Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlvFamtQ%3D%3D&md5=e6be6b245df47fef6730bef44ed044d2CAS |

[59]  D. Thomson, W. Maher, S. Foster, Arsenic and selected elements in inter-tidal and estuarine marine algae, south-east coast, NSW, Australia. Appl. Organomet. Chem. 2007, 21, 396.
Arsenic and selected elements in inter-tidal and estuarine marine algae, south-east coast, NSW, Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXms1yit7s%3D&md5=6ef9ac0d3fb83e09133c52ec0358fb35CAS |

[60]  G. E. Fogg, The Metabolism of Algae 1962 (Wiley: New York).