Register      Login
Environmental Chemistry Environmental Chemistry Society
Environmental problems - Chemical approaches
RESEARCH FRONT (Open Access)

Biosynthesis of arsenolipids by the cyanobacterium Synechocystis sp. PCC 6803

Xi-Mei Xue A B , Georg Raber C , Simon Foster D , Song-Can Chen B E , Kevin A. Francesconi C F and Yong-Guan Zhu A E F
+ Author Affiliations
- Author Affiliations

A Key Laboratory of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, 1799 Jimei Road, Jimei District, Xiamen 361021, China.

B University of Chinese Academy of Sciences, 19A Yuquan Road, Shijingshan District, Beijing 100049, China.

C Institute of Chemistry, University of Graz, Universitaetsplatz 1, A-8010 Graz, Austria.

D Institute for Applied Ecology, University of Canberra, Bruce, ACT 2601, Australia.

E State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, 18 Shuangqing Road, Haidian District, Beijing 100085, China.

F Corresponding authors. Email: ygzhu@iue.ac.cn; kevin.francesconi@uni-graz.at

Environmental Chemistry 11(5) 506-513 https://doi.org/10.1071/EN14069
Submitted: 1 April 2014  Accepted: 19 May 2014   Published: 16 September 2014

Journal Compilation © CSIRO Publishing 2014 Open Access CC BY-NC-ND

Environmental context. Arsenic biotransformation processes play a key role in the cycling of arsenic in aquatic systems. We show that a freshwater cyanobacterium can convert inorganic arsenic into arsenolipids, and the conversion efficiency depends on the arsenic concentration. The role of these novel arsenic compounds remains to be elucidated.

Abstract. Although methylated arsenic and arsenosugars have been verified in various freshwater organisms, lipid-soluble arsenic compounds have not been identified. Here, we report investigations with the model organism cyanobacterium Synechocystis sp. PCC 6803 wild type and ΔarsM (arsenic(III) S-adenosylmethionine methyltransferase) mutant strain, which lacks the enzymes for arsenic methylation cultured in various concentrations of arsenate (AsV). Although Synechocystis accumulated higher arsenic concentrations at the higher exposure levels, the bioaccumulation factor decreased with increasing AsV. The accumulated arsenic in the cells was partitioned into water-soluble and lipid-soluble fractions; lipid-soluble arsenic was found in Synechocystis wild type cells (3–35 % of the total depending on the level of arsenic exposure), but was not detected in Synechocystis ΔarsM mutant strain showing that ArsM was required for arsenolipid biosynthesis. The arsenolipids present in Synechocystis sp. PCC 6803 were analysed by high performance liquid chromatography–inductively coupled plasma–mass spectrometry, high performance liquid chromatography–electrospray mass spectrometry, and high resolution tandem mass spectrometry. The two major arsenolipids were characterised as arsenosugar phospholipids based on their assigned molecular formulas C47H88O14AsP and C47H90O14AsP, and tandem mass spectrometric data demonstrated the presence of the phosphate arsenosugar and acylated glycerol groups.

Additional keyword: arsenic.


References

[1]  K. A. Francesconi, Current perspectives in arsenic environmental and biological research. Environ. Chem. 2005, 2, 141.
Current perspectives in arsenic environmental and biological research.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVCjsrbF&md5=636a54db8909387d076195f7f77418b6CAS |

[2]  S. Miyashita, S. Fujiwara, M. Tsuzuki, T. Kaise, Rapid biotransformation of arsenate into oxo-arsenosugars by a freshwater unicellular green alga, Chlamydomonas reinhardtii. Biosci. Biotechnol. Biochem. 2011, 75, 522.
Rapid biotransformation of arsenate into oxo-arsenosugars by a freshwater unicellular green alga, Chlamydomonas reinhardtii.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltF2lsL8%3D&md5=0a43e84cb7b1bbc4aaad93448d1e83efCAS | 21389618PubMed |

[3]  S. Miyashita, M. Shimoya, Y. Kamidate, T. Kuroiwa, O. Shikino, S. Fujiwara, K. A. Francesconi, T. Kaise, Rapid determination of arsenic species in freshwater organisms from the arsenic-rich Hayakawa River in Japan using HPLC-ICP-MS. Chemosphere 2009, 75, 1065.
Rapid determination of arsenic species in freshwater organisms from the arsenic-rich Hayakawa River in Japan using HPLC-ICP-MS.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltFWltLk%3D&md5=58cb051006e75cd1a9b226558f144598CAS | 19203781PubMed |

[4]  S. Miyashita, S. Fujiwara, M. Tsuzuki, T. Kaise, Cyanobacteria produce arsenosugars. Environ. Chem. 2012, 9, 474.
Cyanobacteria produce arsenosugars.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslSmtrrF&md5=440bbf9f9d60bd4122d8586dcf2fe168CAS |

[5]  A. Geiszinger, W. Goessler, D. Kuehnelt, K. A. Francesconi, W. Kosmus, Determination of arsenic compounds in earthworms. Environ. Sci. Technol. 1998, 32, 2238.
Determination of arsenic compounds in earthworms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXktVyiu7c%3D&md5=dd1cba55b06dbc7d6f2da2c2e8e07dd1CAS |

[6]  G. Lunde, Analysis of arsenic in marine oils by neutron activation. Evidence of arseno organic compounds. J. Am. Oil Chem. Soc. 1968, 45, 331.
Analysis of arsenic in marine oils by neutron activation. Evidence of arseno organic compounds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF1cXktV2isrk%3D&md5=a447755f62f6f38b722cf2e1eece95a8CAS | 5655522PubMed |

[7]  A. Rumpler, S. Edmonds, M. Katsu, K. B. Jensen, W. Goessler, G. Raber, H. Gunnlaugsdottir, K. A. Francesconi, Arsenic-containing long-chain fatty acids in cod-liver oil: a result of biosynthetic infidelity? Angew. Chem. Int. Ed. 2008, 47, 2665.
Arsenic-containing long-chain fatty acids in cod-liver oil: a result of biosynthetic infidelity?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXkvFejsL4%3D&md5=88e2bccbeae33966b484906813471103CAS |

[8]  K. O. Amayo, A. Petursdottir, C. Newcombe, H. Gunnlaugsdottir, A. Raab, E. M. Krupp, J. Feldmann, Identification and quantification of arsenolipids using reversed-phase HPLC coupled simultaneously to high-resolution ICPMS and high-resolution electrospray MS without species-specific standards. Anal. Chem. 2011, 83, 3589.
Identification and quantification of arsenolipids using reversed-phase HPLC coupled simultaneously to high-resolution ICPMS and high-resolution electrospray MS without species-specific standards.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXksFaktL4%3D&md5=87d42103f36c3d43af7866b8d006b1d0CAS | 21446761PubMed |

[9]  G. Raber, S. Khoomrung, M. S. Taleshi, J. S. Edmonds, K. A. Francesconi, Identification of arsenolipids with GC/MS. Talanta 2009, 78, 1215.
Identification of arsenolipids with GC/MS.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjtVSnsL8%3D&md5=65a56bf5ae1ed0244eb0f098aac7bb5bCAS | 19269497PubMed |

[10]  U. Arroyo-Abad, J. Mattusch, S. Mothes, M. Möder, R. Wennrich, M. P. Elizalde-González, F. M. Matysik, Detection of arsenic-containing hydrocarbons in canned cod liver tissue. Talanta 2010, 82, 38.
Detection of arsenic-containing hydrocarbons in canned cod liver tissue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXntVyktbo%3D&md5=a9eb877c83b76e27a5bb4b9978103ee4CAS | 20685432PubMed |

[11]  M. S. Taleshi, J. S. Edmonds, W. Goessler, M. J. Ruiz-Chancho, G. Raber, K. B. Jensen, K. A. Francesconi, Arsenic-containing lipids are natural constituents of sashimi tuna. Environ. Sci. Technol. 2010, 44, 1478.
Arsenic-containing lipids are natural constituents of sashimi tuna.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXptlymtg%3D%3D&md5=865e377839f32f31da0e188a0fd5eb9aCAS | 20099809PubMed |

[12]  M. Morita, Y. Shibata, Isolation and identification of arseno-lipid from a brown alga, Undaria pinnatifida (Wakame). Chemosphere 1988, 17, 1147.
Isolation and identification of arseno-lipid from a brown alga, Undaria pinnatifida (Wakame).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXkvVOlt78%3D&md5=268978f4517d2f3f0bf97a06e7ee7aebCAS |

[13]  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 |

[14]  A. Raab, C. Newcombe, D. Pitton, R. Ebel, J. Feldmann, Comprehensive analysis of lipophilic arsenic species in a brown alga (Saccharina latissima). Anal. Chem. 2013, 85, 2817.
Comprehensive analysis of lipophilic arsenic species in a brown alga (Saccharina latissima).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXit1ehsr0%3D&md5=0716fece190df0381e234715ffd3a833CAS | 23394220PubMed |

[15]  T. Kaneko, A. Tanaka, S. Sato, H. Kotani, T. Sazuka, N. Miyajima, M. Sugiura, S. Tabata, Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. I. Sequence features in the 1 Mb region from map positions 64 % to 92 % of the genome. DNA Res. 1995, 2, 153.
Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. I. Sequence features in the 1 Mb region from map positions 64 % to 92 % of the genome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXptVCrt7o%3D&md5=8e469423f8c448bae5b9f90d72e9493cCAS | 8590279PubMed |

[16]  T. Kaneko, S. Sato, H. Kotani, A. Tanaka, E. Asamizu, Y. Nakamura, N. Miyajima, M. Hirosawa, M. Suquira, S. Sadamoto, T. Kimura, T. Hosouchi, A. Matsuno, A. Muraki, N. Nakazaki, K. Naruo, S. Okumura, S. Shimpo, C. Takeuchi, T. Wada, A. Watanabe, M. Yamada, M. Yasuda, S. Tabata, Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res. 1996, 3, 109.
Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xmtl2qsLc%3D&md5=23b24fff87389e795878d3914f5758c7CAS | 8905231PubMed |

[17]  J. G. Williams, Construction of specific mutations in photosystem II photosynthetic reaction center by genetic engineering methods in Synechocystis 6803. Methods Enzymol. 1988, 167, 766.
Construction of specific mutations in photosystem II photosynthetic reaction center by genetic engineering methods in Synechocystis 6803.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXhvVKqs7g%3D&md5=9d6688b8a949fa3e967263dbf33f43a2CAS |

[18]  R. Rippka, J. Deruelles, J. B. Waterbury, M. Herdman, R. Y. Stanier, Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J. Gen. Microbiol. 1979, 111, 1.
Generic assignments, strain histories and properties of pure cultures of cyanobacteria.Crossref | GoogleScholarGoogle Scholar |

[19]  D. Thomson, W. Maher, S. Foster, Arsenic and selected elements in intertidal and estuarine marine algae, southeast coast, NSW, Australia. Appl. Organomet. Chem. 2007, 21, 396.
Arsenic and selected elements in intertidal and estuarine marine algae, southeast coast, NSW, Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXms1yit7s%3D&md5=71e7b70107e310574ae0c95fa0523870CAS |

[20]  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=fc9c0433f676675f071cfc450fa09bebCAS |

[21]  A. Geiszinger, W. Goessler, S. N. Pedersen, K. A. Francesconi, Arsenic biotransformation by the brown macroalga Fucus serratus. Environ. Toxicol. Chem. 2001, 20, 2255.
Arsenic biotransformation by the brown macroalga Fucus serratus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitlWitQ%3D%3D&md5=e6682d92059a06f67289d901751e1434CAS | 11596758PubMed |

[22]  X. X. Yin, L. H. Wang, R. Bai, H. Huang, G. X. Sun, Accumulation and transformation of arsenic in the blue-green alga Synechocystis sp. PCC 6803. Water Air Soil Pollut. 2012, 223, 1183.
Accumulation and transformation of arsenic in the blue-green alga Synechocystis sp. PCC 6803.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xis1Onsrg%3D&md5=8bac986faadffcc3da5cf5eba51ebcf9CAS |

[23]  B. G. Gamble, J. A. Shoemaker, X. Wei, C. A. Schwegel, J. T. Creed, An investigation of the chemical stability of arsenosugars in simulated gastric juice and acidic environments using IC–ICP-MS and IC-ESI-MS/MS. Analyst 2002, 127, 781.
An investigation of the chemical stability of arsenosugars in simulated gastric juice and acidic environments using IC–ICP-MS and IC-ESI-MS/MS.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktVegsb8%3D&md5=5952bcdb431c23b90a0fc4359f98cafcCAS |

[24]  R. Mukhopadhyay, B. P. Rosen, L. T. Phung, S. Silver, Microbial arsenic: from geocycles to genes and enzymes. FEMS Microbiol. Rev. 2002, 26, 311.
Microbial arsenic: from geocycles to genes and enzymes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmtVamsrg%3D&md5=922fd923fc3fabaf5827e0ad74c8b8e8CAS | 12165430PubMed |

[25]  S. Maeda, S. Nakashima, T. Takeshita, S. Higashi, Bioaccumulation of arsenic by freshwater algae and the application to the removal of inorganic arsenic from an aqueous phase. Part II. By Chlorella vulgaris isolated from arsenic-polluted environment. Sep. Sci. Technol. 1985, 20, 153.
Bioaccumulation of arsenic by freshwater algae and the application to the removal of inorganic arsenic from an aqueous phase. Part II. By Chlorella vulgaris isolated from arsenic-polluted environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXitFKmsrw%3D&md5=3e8db7e003d7a8cf051c83b31df349faCAS |

[26]  L. A. Murray, A. Raab, I. L. Marr, J. Feldmann, Biotransformation of arsenate to arsenosugars by Chlorella vulgaris. Appl. Organomet. Chem. 2003, 17, 669.
Biotransformation of arsenate to arsenosugars by Chlorella vulgaris.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmvFOrtL4%3D&md5=31a86bf4c3f1d252ed5150109fa509cdCAS |

[27]  S. Maeda, S. Fujita, A. Ohki, I. Yoshifuku, S. Higashi, T. Takeshita, Arsenic accumulation by arsenic-tolerant freshwater blue-green alga (Phormidium sp.). Appl. Organomet. Chem. 1988, 2, 353.
Arsenic accumulation by arsenic-tolerant freshwater blue-green alga (Phormidium sp.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXktlCn&md5=c4cb0f25efcf1e5e3f8ba675ad73e83eCAS |

[28]  A. Suhendrayatna, A. Ohki, T. Nakajima, S. Maeda, Studies on the accumulation and transformation of arsenic in freshwater organisms II. Accumulation and transformation of arsenic compounds by Tilapia mossambica. Chemosphere 2002, 46, 325.
Studies on the accumulation and transformation of arsenic in freshwater organisms II. Accumulation and transformation of arsenic compounds by Tilapia mossambica.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXpt1ahsLs%3D&md5=033d14f4c10d7d184b04ba1ae6c39a13CAS |

[29]  D. W. Klumpp, Accumulation of arsenic from water and food by Littorina littoralis and Nucella lapillus. Mar. Biol. 1980, 58, 265.
Accumulation of arsenic from water and food by Littorina littoralis and Nucella lapillus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXkt1aiuw%3D%3D&md5=c6b986c9e0d6d53eba2282a63ec100d1CAS |

[30]  D. S. Tawfik, R. E. Viola, Arsenate replacing phosphate – alternative life chemistries and ion promiscuity. Biochemistry 2011, 50, 1128.
Arsenate replacing phosphate – alternative life chemistries and ion promiscuity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlSmt78%3D&md5=99eb9fa4c3bb56dace71ee807b8eca4eCAS | 21214261PubMed |

[31]  A. A. Meharg, M. R. Macnair, Suppression of the high affinity phosphate uptake system: a mechanism of arsenate tolerance in Holcus lanatus L. J. Exp. Bot. 1992, 43, 519.
Suppression of the high affinity phosphate uptake system: a mechanism of arsenate tolerance in Holcus lanatus L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XisFSis7Y%3D&md5=ba36585b0724f08998760c9d73271179CAS |

[32]  L. López-Maury, A. M. Sánchez-Riego, J. C. Reyes, F. J. Florencio, The glutathione/glutaredoxin system is essential for arsenate reduction in Synechocystis sp. strain PCC 6803. J. Bacteriol. 2009, 191, 3534.
The glutathione/glutaredoxin system is essential for arsenate reduction in Synechocystis sp. strain PCC 6803.Crossref | GoogleScholarGoogle Scholar | 19304854PubMed |

[33]  L. López-Maury, F. J. Florencio, J. C. Reyes, Arsenic sensing and resistance system in the cyanobacterium Synechocystis sp. strain PCC 6803. J. Bacteriol. 2003, 185, 5363.
Arsenic sensing and resistance system in the cyanobacterium Synechocystis sp. strain PCC 6803.Crossref | GoogleScholarGoogle Scholar | 12949088PubMed |

[34]  B. P. Rosen, M. G. Borbolla, A plasmid-encoded arsenite pump produces arsenite resistance in Escherichia coli. Biochem. Biophys. Res. Commun. 1984, 124, 760.
A plasmid-encoded arsenite pump produces arsenite resistance in Escherichia coli.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXhvVCqsw%3D%3D&md5=e0f16a8b5dd36056ade662152d38a4c9CAS | 6391481PubMed |

[35]  H. Bhattacharjee, B. P. Rosen, Arsenic metabolism in prokaryotic and eukaryotic microbes, in Molecular Microbiology of Heavy Metals (Eds D. Nies, S. Silver) 2007, pp. 371–406 (Springer: New York).

[36]  X. Y. Xu, S. P. McGrath, F. J. Zhao, Rapid reduction of arsenate in the medium mediated by plant roots. New Phytol. 2007, 176, 590.
Rapid reduction of arsenate in the medium mediated by plant roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVSisbbO&md5=4f61fd0b2a2c63ba0a5d119cc808a573CAS | 17692074PubMed |

[37]  M. O. Andreae, Distribution and speciation of arsenic in natural waters and some marine algae. Deep-Sea Res. 1978, 25, 391.
Distribution and speciation of arsenic in natural waters and some marine algae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXks1Cqsb4%3D&md5=1d4f356c4b1a7717e90f56e4886440fcCAS |

[38]  A. A. Benson, R. E. Summons, Arsenic accumulation in Great Barrier Reef invertebrates. Science 1981, 211, 482.
Arsenic accumulation in Great Barrier Reef invertebrates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXpslCjug%3D%3D&md5=96afdcc70b2c21136e57e6c9317aa873CAS | 7455685PubMed |