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Australian Journal of Chemistry Australian Journal of Chemistry Society
An international journal for chemical science
RESEARCH ARTICLE

The ascidian Lissoclinum patella, the patellamides and copper

Philipp Baur A , Peter Comba https://orcid.org/0000-0001-7796-3532 A B * , Lawrence R. Gahan C and Christian Scholz D
+ Author Affiliations
- Author Affiliations

A Anorganisch-Chemisches Institut, INF 270, Universität Heidelberg, D-69120 Heidelberg, Germany.

B Interdisziplinäres Zentrum für Wissenschaftliches Rechnen (IWR), INF 270, Universität Heidelberg.

C School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, Qld 4072, Australia.

D Institut für Geowissenschaften, INF 234-236, Universität Heidelberg, D-69120 Heidelberg, Germany.


Handling Editor: Curt Wentrup

Australian Journal of Chemistry 76(1) 44-48 https://doi.org/10.1071/CH22200
Submitted: 20 September 2022  Accepted: 25 October 2022   Published: 9 December 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing.

Abstract

The ascidian species Lissoclinum patella is found, amongst other places, around Heron Island on the Great Barrier Reef, Australia. L. patella has a cyanobacterial symbiont, Prochloron didemni, known to produce various cyclic peptides, including quantities of the cyclic pseudo-octapeptides, the patellamides. Patellamides are of pharmaceutical interest and have attracted the curiosity of coordination chemists because they can form quite stable mono- and di-nuclear transition metal complexes, particularly with copper(ii). For some patellamide derivatives, the binding of two CuII centres is cooperative and solution equilibria involving metal-free peptides, mono- and di-nuclear copper(ii) complexes, and various functions of these complexes have been described. These studies were also driven by the observation that the ascidians possess copper concentrations in excess of that in the seawater around Heron Island, and accumulation factors of approximately 104 have repeatedly been reported. New data presented here, based on inductively coupled plasma atomic emission spectroscopy (ICP-OES) and ICP-mass spectromety (MS) measurements, indicate that the 104 factor is overestimated and a factor >500 and up to approximately 3000 is more realistic.

Keywords: ascidian, biological function, copper concentration, copper(II) complex, cyclic peptide, marine invertebrates, patellamide, prochloron​​​​​​.


References

[1]  G Cox, Comparison of Prochloron from different hosts. I. Structural and ultrastructural characteristics. New Phytol 1986, 104, 429.
         | Comparison of Prochloron from different hosts. I. Structural and ultrastructural characteristics.Crossref | GoogleScholarGoogle Scholar |

[2]  P Comba, N Dovalil, LR Gahan, GR Hanson, M Westphal, Cyclic peptide marine metabolites and CuII. Dalton Trans 2014, 43, 1935.
         | Cyclic peptide marine metabolites and CuII.Crossref | GoogleScholarGoogle Scholar |

[3]  P Baur, M Kühl, P Comba, L Behrendt, Possible functional roles of patellamides in the ascidian-Prochloron symbiosis. Mar Drugs 2022, 20, 119.
         | Possible functional roles of patellamides in the ascidian-Prochloron symbiosis.Crossref | GoogleScholarGoogle Scholar |

[4]  CM Ireland, AR Durso Jr, RA Newman, MP Hacker, Antineoplastic cyclic peptides from the marine tunicate Lissoclinum patella. J Org Chem 1982, 47, 1807.
         | Antineoplastic cyclic peptides from the marine tunicate Lissoclinum patella.Crossref | GoogleScholarGoogle Scholar |

[5]  BM Degnan, CJ Hawkins, MF Lavin, EJ McCaffrey, DL Parry, DJ Watters, Novel cytotoxic compounds from the ascidian Lissoclinum bistratum. J Med Chem 1989, 32, 1354.
         | Novel cytotoxic compounds from the ascidian Lissoclinum bistratum.Crossref | GoogleScholarGoogle Scholar |

[6]  JP Michael, G Pattenden, Marine Metaboliten und die Komplexierung von Metall-Ionen: Tatsachen und Hypothesen. Angew Chem Int Ed Engl 1993, 32, 1.
         | Marine Metaboliten und die Komplexierung von Metall-Ionen: Tatsachen und Hypothesen.Crossref | GoogleScholarGoogle Scholar |

[7]  LR Gahan, RM Cusack, Metal complexes of synthetic cyclic peptides. Polyhedron 2018, 153, 1.
         | Metal complexes of synthetic cyclic peptides.Crossref | GoogleScholarGoogle Scholar |

[8]  BM Degnan, CJ Hawkins, MF Lavin, EJ McCaffrey, DL Parry, AL van den Brenk, DJ Watters, New cyclic peptides with cytotoxic activity from the ascidian Lissoclinum patella. J Med Chem 1989, 32, 1349.
         | New cyclic peptides with cytotoxic activity from the ascidian Lissoclinum patella.Crossref | GoogleScholarGoogle Scholar |

[9]  AL van den Brenk, DP Fairlie, GR Hanson, LR Gahan, CJ Hawkins, A Jones, Binding of Copper(ii) to the Cyclic Octapeptide Patellamide D. Inorg Chem 1994, 33, 2280.
         | Binding of Copper(ii) to the Cyclic Octapeptide Patellamide D.Crossref | GoogleScholarGoogle Scholar |

[10]  EW Schmidt, MS Donia, Life in cellulose houses: symbiotic bacterial biosynthesis of ascidian drugs and drug leads. Curr Opin Biotechnol 2010, 21, 827.
         | Life in cellulose houses: symbiotic bacterial biosynthesis of ascidian drugs and drug leads.Crossref | GoogleScholarGoogle Scholar |

[11]  JB Koehnke, AF Bent, WE Houssen, G Mann, M Jaspars, JH Naismith, The structural biology of patellamide biosynthesis. Curr Opin Struct Biol 2014, 29, 112.
         | The structural biology of patellamide biosynthesis.Crossref | GoogleScholarGoogle Scholar |

[12]  EW Schmidt, JT Nelson, DA Rasko, S Sudek, JA Eisen, MG Haygood, J Ravel, Patellamide A and C biosynthesis by a microcin-like pathway in Prochloron didemni, the cyanobacterial symbiont of Lissoclinum patella. Proc Natl Acad Sci 2005, 102, 7315.
         | Patellamide A and C biosynthesis by a microcin-like pathway in Prochloron didemni, the cyanobacterial symbiont of Lissoclinum patella.Crossref | GoogleScholarGoogle Scholar |

[13]  P García-Reynaga, MS VanNieuwenhze, A New Total Synthesis of Patellamide A. Org Lett 2008, 10, 4621.
         | A New Total Synthesis of Patellamide A.Crossref | GoogleScholarGoogle Scholar |

[14]  P Wipf, Synthetic studies of biologically active marine cyclopeptides. Chem Rev 1995, 95, 2115.
         | Synthetic studies of biologically active marine cyclopeptides.Crossref | GoogleScholarGoogle Scholar |

[15]  P Comba, R Cusack, DP Fairlie, LR Gahan, GR Hanson, U Kazmaier, A Ramlow, The solution structure of a copper(ii) compound of a new cyclic octapeptide by EPR spectroscopy and force field calculations. Inorg Chem 1998, 37, 6721.
         | The solution structure of a copper(ii) compound of a new cyclic octapeptide by EPR spectroscopy and force field calculations.Crossref | GoogleScholarGoogle Scholar |

[16]  G Haberhauer, F Rominger, Syntheses and Structures of Imidazole Analogues of Lissoclinum Cyclopeptides. Eur J Org Chem 2003, 2003, 3209.
         | Syntheses and Structures of Imidazole Analogues of Lissoclinum Cyclopeptides.Crossref | GoogleScholarGoogle Scholar |

[17]  P Baur, P Comba, G Velmurugan, Efficient synthesis for a wide variety of patellamide derivatives and phosphatase activity of copper–patellamide complexes. Chem Eur J 2022, 28, e202200249.
         | Efficient synthesis for a wide variety of patellamide derivatives and phosphatase activity of copper–patellamide complexes.Crossref | GoogleScholarGoogle Scholar |

[18]  AL van den Brenk, KA Byriel, DP Fairlie, LR Gahan, GR Hanson, CJ Hawkins, A Jones, CHL Kennard, B Moubaraki, KS Murray, Crystal Structure, Electrospray Ionization Mass Spectrometry, Electron Paramagnetic Resonance, and Magnetic Susceptibility Study of [Cu2(asidH2)(1,2-μ-CO3)(H2O)2] 2H2O, the Bis(copper(ii)) Complex of Ascidiacyclamide (ascidH4), a Cyclic Peptide Isolated from the Ascidian Lissoclinum patella. Inorg Chem 1994, 33, 3549.
         | Crystal Structure, Electrospray Ionization Mass Spectrometry, Electron Paramagnetic Resonance, and Magnetic Susceptibility Study of [Cu2(asidH2)(1,2-μ-CO3)(H2O)2] 2H2O, the Bis(copper(ii)) Complex of Ascidiacyclamide (ascidH4), a Cyclic Peptide Isolated from the Ascidian Lissoclinum patella.Crossref | GoogleScholarGoogle Scholar |

[19]  P Comba, N Dovalil, G Haberhauer, K Kowski, N Mehrkens, M Westphal, Copper solution chemistry of cyclic pseudo-octapeptides. Z Anorg Allg Chem 2013, 639, 1395.
         | Copper solution chemistry of cyclic pseudo-octapeptides.Crossref | GoogleScholarGoogle Scholar |

[20]  P Comba, N Dovalil, LR Gahan, G Haberhauer, GR Hanson, CJ Noble, B Seibold, P Vadivelu, CuII coordination chemistry of patellamide derivatives. Possible biological functions of cyclic pseudo-peptides. Chem Eur J 2012, 18, 2578.
         | CuII coordination chemistry of patellamide derivatives. Possible biological functions of cyclic pseudo-peptides.Crossref | GoogleScholarGoogle Scholar |

[21]  PV Bernhardt, P Comba, TW Hambley, SS Massoud, S Stebler, Determination of solution structures of binuclear copper(ii) complexes. Inorg Chem 1992, 31, 2644.
         | Determination of solution structures of binuclear copper(ii) complexes.Crossref | GoogleScholarGoogle Scholar |

[22]  R Latifi, M Bagherzadeh, BF Milne, M Jaspars, SP De Visser, Density functional theory studies of oxygen and carbonate binding to a dicopper patellamide complex. J Inorg Biochem 2008, 102, 2171.
         | Density functional theory studies of oxygen and carbonate binding to a dicopper patellamide complex.Crossref | GoogleScholarGoogle Scholar |

[23]  P Comba, LR Gahan, GR Hanson, M Maeder, M Westphal, Carbonic anhydrase activity of dinuclear CuII complexes with patellamide model ligands. Dalton Trans 2014, 43, 3144.
         | Carbonic anhydrase activity of dinuclear CuII complexes with patellamide model ligands.Crossref | GoogleScholarGoogle Scholar |

[24]  P Comba, LR Gahan, GR Hanson, M Westphal, Phosphatase reactivity of a dicopper(ii) complex of a patellamide derivative – possible biological functions of cyclic pseudopeptides. Chem Commun 2012, 48, 9364.
         | Phosphatase reactivity of a dicopper(ii) complex of a patellamide derivative – possible biological functions of cyclic pseudopeptides.Crossref | GoogleScholarGoogle Scholar |

[25]  P Comba, A Eisenschmidt, N Kipper, J Schießl, Glycosidase- and β-lactamase-like activity of dinuclear copper(ii) patellamide complexes. J Inorg Biochem 2016, 159, 70.
         | Glycosidase- and β-lactamase-like activity of dinuclear copper(ii) patellamide complexes.Crossref | GoogleScholarGoogle Scholar |

[26]  P Comba, A Eisenschmidt, LR Gahan, D-P Herten, G Nette, G Schenk, M Seefeld, Is CuII coordinated to patellamides inside Prochloron cells? Chem Eur J 2017, 23, 12264.
         | Is CuII coordinated to patellamides inside Prochloron cells?Crossref | GoogleScholarGoogle Scholar |

[27]  DJ Freeman, G Pattenden, AF Drake, G Siligardi, Marine metabolites and metal ion chelation. Circular dichroism studies of metal binding to Lissoclinum cyclopeptides. J Chem Soc, Perkin Trans 2 1998, 129.
         | Marine metabolites and metal ion chelation. Circular dichroism studies of metal binding to Lissoclinum cyclopeptides.Crossref | GoogleScholarGoogle Scholar |

[28]  LA Morris, M Jaspars, JJ Kettenes-van den Bosch, K Versluis, AJR Heck, SM Kelly, NC Price, Metal binding of Lissoclinum patella metabolites. Part 1: Patellamides A, C and ulithiacyclamide A. Tetrahedron 2001, 57, 3185.
         | Metal binding of Lissoclinum patella metabolites. Part 1: Patellamides A, C and ulithiacyclamide A.Crossref | GoogleScholarGoogle Scholar |

[29]  GRW Denton, C Burdon-Jones, Trace metals in fish from the Great Barrier Reef. Mar Pollut Bull 1986, 17, 201.
         | Trace metals in fish from the Great Barrier Reef.Crossref | GoogleScholarGoogle Scholar |

[30]  R Tzafriri-Milo, T Benaltabet, A Torfstein, N Shenkar, The Potential Use of Invasive Ascidians for Biomonitoring Heavy Metal Pollution. Front Mar Sci 2019, 6, 611.
         | The Potential Use of Invasive Ascidians for Biomonitoring Heavy Metal Pollution.Crossref | GoogleScholarGoogle Scholar |

[31]  Baur P, Comba P. work in progress.

[32]  PA Yeats, JA Campbell, Nickel, copper, cadmium and zinc in the North-West Atlantic Ocean. Mar Chem 1983, 12, 43.
         | Nickel, copper, cadmium and zinc in the North-West Atlantic Ocean.Crossref | GoogleScholarGoogle Scholar |

[33]  LG Danielsson, B Magnusson, S Westerlund, Cadmium, copper, iron, nickel and zinc in the North-East Atlantic Ocean. Mar Chem 1985, 17, 23.
         | Cadmium, copper, iron, nickel and zinc in the North-East Atlantic Ocean.Crossref | GoogleScholarGoogle Scholar |

[34]  KH Coale, KW Bruland, Copper complexation in the Northeast Pacific. Limnol Oceanogr 1988, 33, 1084.
         | Copper complexation in the Northeast Pacific.Crossref | GoogleScholarGoogle Scholar |

[35]  Blossom N. Copper in the ocean environment. American Chemet Corporation; 2001.

[36]  A-HAM Ali, MA Hamed, HA El-Azim, Heavy metals distribution in the coral reef ecosystems of the Northern Red Sea. Helgol Mar Res 2011, 65, 67.
         | Heavy metals distribution in the coral reef ecosystems of the Northern Red Sea.Crossref | GoogleScholarGoogle Scholar |

[37]  S Takano, M Tanimizu, T Hirata, Y Sohrin, Isotopic constraints on biogeochemical cycling of copper in the ocean. Nat Commun 2014, 5, 5663.
         | Isotopic constraints on biogeochemical cycling of copper in the ocean.Crossref | GoogleScholarGoogle Scholar |

[38]  PP Leal, CL Hurd, SG Sander, E Armstrong, PA Fernández, TJ Suhrhoff, MY Roleda, Copper pollution exacerbates the effects of ocean acidification and warming on kelp microscopic early life stages. Sci Rep 2018, 8, 14763.
         | Copper pollution exacerbates the effects of ocean acidification and warming on kelp microscopic early life stages.Crossref | GoogleScholarGoogle Scholar |