Coralline algal calcification: A morphological and process-based understanding

English version

Autoři: Merinda C. Nash ^aff001; Guillermo Diaz-Pulido ^aff003; Adela S. Harvey ^aff004; Walter Adey ^aff001
Působiště autorů: Department of Botany, National Museum of Natural History, Smithsonian Institution, Washington DC, United States of America ^aff001; Research School of Earth Sciences, Australian National University, Canberra, ACT, Australia ^aff002; Griffith School of Environment and Science, and Australian Rivers Institute, Coast and Estuaries, Nathan Campus, Griffith University, Nathan, Queensland, Australia ^aff003; Department of Ecology, Environment and Evolution, La Trobe University, Bundoora, Victoria, Australia ^aff004
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0221396

Souhrn

Research purpose and findings

Coralline algae are key biological substrates of many carbonate systems globally. Their capacity to build enduring crusts that underpin the formation of tropical reefs, rhodolith beds and other benthic substrate is dependent on the formation of a calcified thallus. However, this important process of skeletal carbonate formation is not well understood. We undertook a study of cellular carbonate features to develop a model for calcification. We describe two types of cell wall calcification; 1) calcified primary cell wall (PCW) in the thin-walled elongate cells such as central medullary cells in articulated corallines and hypothallial cells in crustose coralline algae (CCA), 2) calcified secondary cell wall (SCW) with radial Mg-calcite crystals in thicker-walled rounded cortical cells of articulated corallines and perithallial cells of CCA. The distinctive banding found in many rhodoliths is the regular transition from PCW-only cells to SCW cells. Within the cell walls there can be bands of elevated Mg with Mg content of a few mol% higher than radial Mg-calcite (M-type), ranging up to dolomite composition (D-type).

Model for calcification

We propose the following three-step model for calcification. 1) A thin (< 0.5 μm) PCW forms and is filled with a mineralising fluid of organic compounds and seawater. Nanometer-scale Mg-calcite grains precipitate on the organic structures within the PCW. 2) Crystalline cellulose microfibrils (CMF) are extruded perpendicularly from the cellulose synthase complexes (CSC) in the plasmalemma to form the SCW. 3) The CMF soaks in the mineralising fluid as it extrudes and becomes calcified, retaining the perpendicular form, thus building the radial calcite. In Clathromorphum, SCW formation lags PCW creating a zone of weakness resulting in a split in the sub-surface crust. All calcification seems likely to be a bioinduced rather than controlled process. These findings are a substantial step forward in understanding how corallines calcify.

Klíčová slova:

Cell walls – Algae – Sea water – Cellulose – Calcification – Plant cell walls – Carbonates – Secondary cells

Zdroje

1. Adey WH, Macintyre IG. Crustose Coralline Algae: A Re-evaluation in the Geological Sciences. Geol Soc Am Bull. 1973 Mar 1;84(3):883–904.

2. Riosmena-Rodríguez R. Natural History of Rhodolith/Maërl Beds: Their Role in Near-Shore Biodiversity and Management. In: Riosmena-Rodríguez R, Nelson W, Aguirre J, editors. Rhodolith/Maërl Beds: A Global Perspective [Internet]. Springer International Publishing; 2017 [cited 2017 Jun 25]. p. 3–26. (Coastal Research Library). Available from: http://link.springer.com/chapter/10.1007/978-3-319-29315-8_1

3. James NP, Wray JL, Ginsburg RN. Calcification of Encrusting Aragonitic Algae (Peyssonneliaceae): Implications for the Origin of Late Paleozoic Reefs and Cements. J Sediment Res [Internet]. 1988 [cited 2017 Aug 28];58(2). Available from: http://archives.datapages.com/data/sepm/journals/v55-58/data/058/058002/0291.htm

4. Nash MC, Russell BD, Dixon KR, Liu M, Xu H. Discovery of the mineral brucite (magnesium hydroxide) in the tropical calcifying alga Polystrata dura (Peyssonneliales, Rhodophyta). J Phycol. 2015 Jun 1;51(3):403–7. doi: 10.1111/jpy.12299 26986657

5. Dutra E, Koch M, Peach K, Manfrino C. Tropical crustose coralline algal individual and community responses to elevated pCO2 under high and low irradiance. ICES J Mar Sci. 2016 Mar 1;73(3):803–13.

6. Cabioch J, Giraud G. Structural aspects of biomineralization in the coralline algae (calcified Rhodophyceae). In: Biomineralization in lower plants and animals. 1986. p. 141–56.

7. Ries JB. Mg fractionation in crustose coralline algae: Geochemical, biological, and sedimentological implications of secular variation in the Mg/Ca ratio of seawater. Geochim Cosmochim Acta. 2006 Feb 15;70(4):891–900.

8. Nash MC, Troitzsch U, Opdyke BN, Trafford JM, Russell BD, Kline DI. First discovery of dolomite and magnesite in living coralline algae and its geobiological implications. Biogeosciences. 2011 Nov 15;8(11):3331–40.

9. Adey WH. Review—Coral Reefs: Algal Structured and Mediated Ecosystems in Shallow, Turbulent, Alkaline Waters. J Phycol. 1998 Jun 1;34(3):393–406.

10. Nash MC. Assessing ocean acidification impacts on the reef building properties of crustose coralline algae [Doctorate]. [Canberra, Australia]: Australian National University; 2016.

11. Goreau TF. Calcium Carbonate Deposition by Coralline Algae and Corals in Relation to Their Roles as Reef-Builders. Ann N Y Acad Sci. 1963 May 1;109(1):127–67.

12. Littler MM, Doty MS. Ecological Components Structuring the Seaward Edges of Tropical Pacific Reefs: The Distribution, Communities and Productivity of Porolithon. J Ecol. 1975;63(1):117–29.

13. Adey WH. Coral Reef Morphogenesis: A Multidimensional Model. Science. 1978 Nov 24;202(4370):831–7. doi: 10.1126/science.202.4370.831 17752443

14. Adey WH, Halfar J, Williams B. The Coralline Genus Clathromorphum Foslie emend. Adey. Biological, Physiological, and Ecological Factors Controlling Carbonate Production in an Arctic-Subarctic Climate Archive. Smithson Inst Sch Press. 2013;40:1–39.

15. Amado-Filho GM, Maneveldt G, Manso RCC, Marins-Rosa BV, Pacheco MR, Guimaraes S. Structure of rhodolith beds from 4 to 55 meters deep along the southern coast of Espírito Santo State, Brazil. Cienc Mar. 2007 Dec 4;33(4):399–410.

16. Harvey AS, Harvey RM, Merton E. The distribution, significance and vulnerability of Australian rhodolith beds: a review. Mar Freshw Res. 2016 May 16;68(3):411–28.

17. Darrenougue N, De Deckker P, Eggins S, Payri C. Sea-surface temperature reconstruction from trace elements variations of tropical coralline red algae. Quat Sci Rev. 2014 Jun 1;93:34–46.

18. Kamenos NA, Cusack M, Moore PG. Coralline algae are global palaeothermometers with bi-weekly resolution. Geochim Cosmochim Acta. 2008 Feb 1;72(3):771–9.

19. Foster M. RHODOLITHS: BETWEEN ROCKS AND SOFT PLACES. J Phycol. 2001;37:659–67.

20. Underwood AJ, Chapman MG. Variation in algal assemblages on wave-exposed rocky shores in New South Wales. Mar Freshw Res. 1998 Jul 21;49(3):241–54.

21. Bussell JA, Lucas IAN, Seed R. Patterns in the invertebrate assemblage associated with <span class = “italic”>Corallina officinalis in tide pools. J Mar Biol Assoc U K. 2007 Apr;87(2):383–8.

22. Fisher K, Martone PT. Field Study of Growth and Calcification Rates of Three Species of Articulated Coralline Algae in British Columbia, Canada. Biol Bull. 2014 Apr 1;226(2):121–30. doi: 10.1086/BBLv226n2p121 24797094

23. Halfar J, Steneck R, Schöne B, Moore GWK, Joachimski M, Kronz A, et al. Coralline alga reveals first marine record of subarctic North Pacific climate change. Geophys Res Lett. 2007 Apr 1;34(7):L07702.

24. Williams B, Halfar J, Steneck RS, Wortmann UG, Hetzinger S, Adey W, et al. Twentieth century δ13C variability in surface water dissolved inorganic carbon recorded by coralline algae in the northern North Pacific Ocean and the Bering Sea. Biogeosciences. 2011 Jan 24;8(1):165–74.

25. Chan P, Halfar J, Adey W, Hetzinger S, Zack T, Moore GWK, et al. Multicentennial record of Labrador Sea primary productivity and sea-ice variability archived in coralline algal barium. Nat Commun [Internet]. 2017 Jun 1;8. Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5461504/

26. Sletten HR, Andrus CFT, Guzmán HM, Halfar J. Re-evaluation of using rhodolith growth patterns for paleoenvironmental reconstruction: An example from the Gulf of Panama. Palaeogeogr Palaeoclimatol Palaeoecol. 2017 Jan 1;465, Part A:264–77.

27. Ries JB. Skeletal mineralogy in a high-CO2 world. J Exp Mar Biol Ecol. 2011 Jul 15;403(1–2):54–64.

28. Hofmann LC, Yildiz G, Hanelt D, Bischof K. Physiological responses of the calcifying rhodophyte, Corallina officinalis (L.), to future CO2 levels. Mar Biol. 2012 Apr 1;159(4):783–92.

29. Egilsdottir H, Noisette F, Noël LM-LJ, Olafsson J, Martin S. Effects of pCO2 on physiology and skeletal mineralogy in a tidal pool coralline alga Corallina elongata. Mar Biol. 2013 Aug 1;160(8):2103–12.

30. Diaz-Pulido G, Nash MC, Anthony KRN, Bender D, Opdyke BN, Reyes-Nivia C, et al. Greenhouse conditions induce mineralogical changes and dolomite accumulation in coralline algae on tropical reefs. Nat Commun. 2014 Feb 12;5:3310. doi: 10.1038/ncomms4310 24518160

31. Fietzke J, Ragazzola F, Halfar J, Dietze H, Foster LC, Hansteen TH, et al. Century-scale trends and seasonality in pH and temperature for shallow zones of the Bering Sea. Proc Natl Acad Sci. 2015 Mar 10;112(10):2960–5. doi: 10.1073/pnas.1419216112 25713385

32. Kamenos NA, Perna G, Gambi MC, Micheli F, Kroeker KJ. Coralline algae in a naturally acidified ecosystem persist by maintaining control of skeletal mineralogy and size. Proc R Soc B. 2016 Oct 12;283(1840):20161159. doi: 10.1098/rspb.2016.1159 27733544

33. Lewis B, Kennedy EV, Diaz-Pulido G. Seasonal growth and calcification of a reef-building crustose coralline alga on the Great Barrier Reef. Mar Ecol Prog Ser. 2017;568:73–86.

34. Johnson MD, Moriarty VW, Carpenter RC. Acclimatization of the Crustose Coralline Alga Porolithon onkodes to Variable pCO2. PLOS ONE. 2014 Feb 5;9(2):e87678. doi: 10.1371/journal.pone.0087678 24505305

35. Hurd CL, Cornwall CE, Currie K, Hepburn CD, McGraw CM, Hunter KA, et al. Metabolically induced pH fluctuations by some coastal calcifiers exceed projected 22nd century ocean acidification: a mechanism for differential susceptibility? Glob Change Biol. 2011 Oct 1;17(10):3254–62.

36. Cornwall CE, Boyd PW, McGraw CM, Hepburn CD, Pilditch CA, Morris JN, et al. Diffusion Boundary Layers Ameliorate the Negative Effects of Ocean Acidification on the Temperate Coralline Macroalga Arthrocardia corymbosa. PLOS ONE. 2014 May 13;9(5):e97235. doi: 10.1371/journal.pone.0097235 24824089

37. Hofmann LC, Koch M, Beer D de. Biotic Control of Surface pH and Evidence of Light-Induced H+ Pumping and Ca2+-H+ Exchange in a Tropical Crustose Coralline Alga. PLOS ONE. 2016 Jul 26;11(7):e0159057. doi: 10.1371/journal.pone.0159057 27459463

38. Nash MC, Adey W. Anatomical structure overrides temperature controls on magnesium uptake—calcification in the arctic/subarctic coralline algae Leptophytum laeve and Kvaleya epilaeve (Rhodophyta; Corallinales). Biogeosciences. 2018;15(3),781–795.

39. Nash MC, Adey W. Multiple phases of mg-calcite in crustose coralline algae suggest caution for temperature proxy and ocean acidification assessment: lessons from the ultrastructure and biomineralisation in Phymatolithon (Rhodophyta, Corallinales). J Phycol. 2017;53(5),970–984. doi: 10.1111/jpy.12559 28671731

40. Cornwall CE, Comeau S, McCulloch M. Coralline algae elevate pH at the site of calcification under ocean acidification. Glob Change Biol. 2017;00:1–12.

41. Chisholm JRM. Primary productivity of reef-building crustose coralline algae. Limnol Oceanogr. 2003;48(4):1376–87.

42. Borowitzka MA, Larkum AWD. Calcification in the Green Alga HalimedaIII. THE SOURCES OF INORGANIC CARBON FOR PHOTOSYNTHESIS AND CALCIFICATION AND A MODEL OF THE MECHANISM OF CALCIFICATION. J Exp Bot. 1976 Oct 1;27(5):879–93.

43. Borowitzka MA. Calcification in aquatic plants. Plant Cell Environ. 1984;7:457–66.

44. Lee D, Carpenter SJ. Isotopic disequilibrium in marine calcareous algae. Chem Geol. 2001 Feb 15;172(3–4):307–29.

45. Borowitzka MA. Photosynthesis and calcification in the articulated coralline red algae Amphiroa anceps and A. foliacea. Mar Biol. 1981 Apr 1;62(1):17–23.

46. Adey WH, Sperapani CP. The biology of Kvaleya epilaeve, a new parasitic genus and species of Corallinaceae. Phycologia. 1971 Mar 1;10(1):29–42.

47. Adey W, Masaki T, Akioka H. Ezo epiyessoense, A New Parasitic Genus and Species of Corallinaceae. Phycologia. 1974;13:329–44.

48. Halfar J, Adey WH, Kronz A, Hetzinger S, Edinger E, Fitzhugh WW. Arctic sea-ice decline archived by multicentury annual-resolution record from crustose coralline algal proxy. Proc Natl Acad Sci. 2013 Dec 3;110(49):19737–41. doi: 10.1073/pnas.1313775110 24248344

49. Adey W, Hernandez-Kantun J, Gabrielson P, Nash M, Hayek L. Phymatolithon (Melobesioideae, Hapalidiales) in the Boreal-Subarctic transition zone of the North Atlantic: a correlation of plastid DNA markers with morpho-anatomy, ecology and biogeography. Smithson Inst Sch Press. 2017;In press:Forthcoming.

50. McCulloch M, Falter J, Trotter J, Montagna P. Coral resilience to ocean acidification and global warming through pH up-regulation. Nat Clim Change. 2012 Aug;2(8):623–7.

51. Cohen AL, McConnaughey TA. Geochemical Perspectives on Coral Mineralization. Rev Mineral Geochem. 2003 Jan 3;54(1):151–87.

52. Allemand D, Ferrier-Pagès C, Furla P, Houlbrèque F, Puverel S, Reynaud S, et al. Biomineralisation in reef-building corals: from molecular mechanisms to environmental control. Comptes Rendus Palevol. 2004 Oct 1;3(6):453–67.

53. Von Euw S, Zhang Q, Manichev V, Murali N, Gross J, Feldman LC, et al. Biological control of aragonite formation in stony corals. Science. 2017 Jun 2;356(6341):933–8. doi: 10.1126/science.aam6371 28572387

54. Wanamaker AD Jr., Hetzinger S, Halfar J. Reconstructing mid- to high-latitude marine climate and ocean variability using bivalves, coralline algae, and marine sediment cores from the Northern Hemisphere. Palaeogeogr Palaeoclimatol Palaeoecol. 2011 Mar 1;302(1–2):1–9.

55. de Nooijer LJ, Spero HJ, Erez J, Bijma J, Reichart GJ. Biomineralization in perforate foraminifera. Earth-Sci Rev. 2014 Aug;135:48–58.

56. Gross E, Wernberg T, Terrados J. What is a plant? and what is aquatic botany? Aquat Bot. 2016;132(3–4).

57. Bolton JJ. What is aquatic botany?—And why algae are plants: The importance of non-taxonomic terms for groups of organisms. Aquat Bot. 2016 Jul 1;132(Supplement C):1–4.

58. Adey WH. The Genus Phymatolithon in the Gulf of Main. Hydrobiologia. 1964;24(1–2):377–420.

59. Adey W. The Genus Clathromorphum in the Gulf of Maine. Hydrobiologia. 1965;26:539–73.

60. Adey WH, Chamberlain YM, Irvine LM. An Sem-Based Analysis of the Morphology, Anatomy, and Reproduction of Lithothamnion Tophiforme (esper) Unger (corallinales, Rhodophyta), with a Comparative Study of Associated North Atlantic Arctic/Subarctic Melobesioideae1. J Phycol. 2005 Oct 1;41(5):1010–24.

61. Steneck RS. The Ecology of Coralline Algal Crusts: Convergent Patterns and Adaptative Strategies. Annu Rev Ecol Syst. 1986;17(1):273–303.

62. Matty PJ, Johansen HW. A histochemical study of Corallina officinalis (Rhodophyta, Corallinaceae). Phycologia. 1981 Mar 1;20(1):46–55.

63. Harvey AS, Woelkerling WJ, Millar A. The Genus Amphiroa (Lithophylloideae, Corallinaceae, Rhodophyta) from the Temperate Coasts of the Australian Continent, Including the Newly Described A. klochkovana. Phycologia. 2009 Jul 6;48(4):258–90.

64. Borowitzka MA, Larkum AWD, Nockolds CE. A scanning electron microscope study of the structure and organization of the calcium carbonate deposits of algae. Phycologia. 1974 Sep 1;13(3):195–203.

65. Stanley SM, Ries JB, Hardie LA. Low-magnesium calcite produced by coralline algae in seawater of Late Cretaceous composition. Proc Natl Acad Sci. 2002 Nov 26;99(24):15323–6. doi: 10.1073/pnas.232569499 12399549

66. Evert RF. Esau’s Plant Anatomy: Meristems, Cells, and Tissues of the Plant Body: Their Structure, Function, and Development. John Wiley & Sons; 2006. 624 p.

67. Nakano Y, Yamaguchi M, Endo H, Rejab NA, Ohtani M. NAC-MYB-based transcriptional regulation of secondary cell wall biosynthesis in land plants. Front Plant Sci [Internet]. 2015 [cited 2017 Feb 19];6. Available from: http://journal.frontiersin.org/article/10.3389/fpls.2015.00288/abstract

68. Campbell N, Reece J, Mitchell L. Biology. 5th ed. CA: Benjamin Cummings; 1999. 570 p.

69. Diotallevi F, Mulder B. The Cellulose Synthase Complex: A Polymerization Driven Supramolecular Motor. Biophys J. 2007 Apr 15;92(8):2666–73. doi: 10.1529/biophysj.106.099473 17237206

70. Tsekos I. The Sites of Cellulose Synthesis in Algae: Diversity and Evolution of Cellulose-Synthesizing Enzyme Complexes. J Phycol. 1999 Aug 1;35(4):635–55.

71. Popper Z, Gurvan M, Herve Cecile, Domozych David S., Willats William G. T., Tuohy Maria G., et al. Evolution and Diversity of Plant Cell Walls: From Algae to Flowering Plants. Annu Rev Plant Biol. 2011;62(1):567–90.

72. Paredez AR, Somerville CR, Ehrhardt DW. Visualization of Cellulose Synthase Demonstrates Functional Association with Microtubules. Science. 2006 Jun 9;312(5779):1491–5. doi: 10.1126/science.1126551 16627697

73. Rafsanjani A, Stiefel M, Jefimovs K, Mokso R, Derome D, Carmeliet J. Hygroscopic swelling and shrinkage of latewood cell wall micropillars reveal ultrastructural anisotropy. J R Soc Interface. 2014 Jun 6;11(95):20140126. doi: 10.1098/rsif.2014.0126 24671938

74. Mellerowicz EJ, Sundberg B. Wood cell walls: biosynthesis, developmental dynamics and their implications for wood properties. Curr Opin Plant Biol. 2008 Jun;11(3):293–300. doi: 10.1016/j.pbi.2008.03.003 18434240

75. Martone PT, Estevez JM, Lu F, Ruel K, Denny MW, Somerville C, et al. Discovery of Lignin in Seaweed Reveals Convergent Evolution of Cell-Wall Architecture. Curr Biol. 2009 Jan 27;19(2):169–75. doi: 10.1016/j.cub.2008.12.031 19167225

76. Buchanan B, Gruissem W, Jones R. Biochemistry and Molecular Biology of Plants edited by Buchanan Bob B., Gruissem Wilhelm, Jones Russell L. Second. UK: Wiley and Sons; 2015.

77. Cosgrove D. Growth of the plant cell wall. Nature. 2005;6:850–61.

78. Cole KM, Sheath RG. Biology of the Red Algae. Cambridge University Press; 1990. 530 p.

79. Bilan MI, Usov AI. Polysaccharides of Calcareous Algae and Their Effect on the Calcification Process. Russ J Bioorganic Chem. 2001 Jan 1;27(1):2–16.

80. Martone PT, Navarro DA, Stortz CA, Estevez JM. Differences in Polysaccharide Structure Between Calcified and Uncalcified Segments in the Coralline Calliarthron Cheilosporioides (corallinales, Rhodophyta)1. J Phycol. 2010 Jun 1;46(3):507–15.

81. Navarro DA, Ricci AM, Rodríguez MC, Stortz CA. Xylogalactans from Lithothamnion heterocladum, a crustose member of the Corallinales (Rhodophyta). Carbohydr Polym. 2011 Mar 17;84(3):944–51.

82. Malagoli BG, Cardozo FTGS, Gomes JHS, Ferraz VP, Simões CMO, Braga FC. Chemical characterization and antiherpes activity of sulfated polysaccharides from Lithothamnion muelleri. Int J Biol Macromol. 2014 May;66:332–7. doi: 10.1016/j.ijbiomac.2014.02.053 24608026

83. Okazaki M, Furuya K, Tsukayama K, Nisizawa K. Isolation and Identification of Alginic Acid from a Calcareous Red Alga Serraticardia maxima. Bot Mar. 2009;25(3):123–32.

84. Rees DA, Welsh EJ. Secondary and Tertiary Structure of Polysaccharides in Solutions and Gels. Angew Chem Int Ed Engl. 1977 Apr 1;16(4):214–24.

85. Rahman MA, Halfar J. First evidence of chitin in calcified coralline algae: new insights into the calcification process of Clathromorphum compactum. Sci Rep. 2014 Aug 22;4:6162. doi: 10.1038/srep06162 25145331

86. Barbosa MA, Granja PL, Barrias CC, Amaral IF. Polysaccharides as scaffolds for bone regeneration. ITBM-RBM. 2005 Jun;26(3):212–7.

87. Venkatesan J, Bhatnagar I, Manivasagan P, Kang K-H, Kim S-K. Alginate composites for bone tissue engineering: A review. Int J Biol Macromol. 2015 Jan;72:269–81. doi: 10.1016/j.ijbiomac.2014.07.008 25020082

88. Venkatesan J, Lowe B, Anil S, Manivasagan P, Kheraif AAA, Kang K-H, et al. Seaweed polysaccharides and their potential biomedical applications. Starch—Stärke. 2015 May 1;67(5–6):381–90.

89. Stoppel WL, Ghezzi CE, McNamara SL, Iii LDB, Kaplan DL. Clinical Applications of Naturally Derived Biopolymer-Based Scaffolds for Regenerative Medicine. Ann Biomed Eng. 2015 Mar 1;43(3):657–80. doi: 10.1007/s10439-014-1206-2 25537688

90. Shen X L. Shamshina J, Berton P, Gurau G, Rogers R D. Hydrogels based on cellulose and chitin: fabrication, properties, and applications. Green Chem. 2016;18(1):53–75.

91. Granja PL, Ribeiro CC, Jéso BD, Baquey C, Barbosa MA. Mineralization of regenerated cellulose hydrogels. J Mater Sci Mater Med. 2001 Sep 1;12(9):785–91. 15348225

92. Märtson M, Viljanto J, Hurme T, Saukko P. Biocompatibility of Cellulose Sponge with Bone. Eur Surg Res. 1998 Dec 9;30(6):426–32. doi: 10.1159/000008609 9838236

93. de Araújo Júnior AM, Braido G, Saska S, Barud HS, Franchi LP, Assunção RMN, et al. Regenerated cellulose scaffolds: Preparation, characterization and toxicological evaluation. Carbohydr Polym. 2016 Jan 20;136:892–8. doi: 10.1016/j.carbpol.2015.09.066 26572426

94. Cox TE, Nash M, Gazeau F, Déniel M, Legrand E, Alliouane S, et al. Effects of in situ CO2 enrichment on Posidonia oceanica epiphytic community composition and mineralogy. Mar Biol. 2017 Apr 9;5(164):1–16.

95. Gregg JM, Bish DL, Kaczmarek SE, Machel HG. Mineralogy, nucleation and growth of dolomite in the laboratory and sedimentary environment: A review. Sedimentology. 2015 Oct 1;62(6):1749–69.

96. Zhang F, Xu H, Shelobolina ES, Konishi H, Converse B, Shen Z, et al. The catalytic effect of bound extracellular polymeric substances excreted by anaerobic microorganisms on Ca-Mg carbonate precipitation: Implications for the “dolomite problem.” Am Mineral. 2015;100(2–3):483–94.

97. Nash MC, Martin S, Gattuso J-P. Mineralogical response of the Mediterranean crustose coralline alga Lithophyllum cabiochae to near-future ocean acidification and warming. Biogeosciences. 2016 Nov 1;13(21):5937–45.

98. Halfar J, Steneck RS, Joachimski M, Kronz A, Wanamaker AD. Coralline red algae as high-resolution climate recorders. Geology. 2008 Jun 1;36(6):463–6.

99. Raz S, Weiner S, Addadi L. Formation of High-Magnesian Calcites via an Amorphous Precursor Phase: Possible Biological Implications. Adv Mater. 2000 Jan 1;12(1):38–42.

100. Zhang F, Xu H, Konishi H, Shelobolina ES, Roden E. Polysaccharide-catalyzed nucleation and growth of disordered dolomite: A potential precursor of sedimentary dolomite. Am Mineral. 2012;97(4):556–67.

101. Merk V, Chanana M, Keplinger T, Gaan S, Burgert I. Hybrid wood materials with improved fire retardance by bio-inspired mineralisation on the nano- and submicron level. Green Chem. 2015;17(3):1423–8.

102. Weiner S, Dove PM. An Overview of Biomineralization Processes and the Problem of the Vital Effect. Rev Mineral Geochem. 2003 Jan 3;54(1):1–29.

103. Addadi L, Weiner S. Biomineralization: mineral formation by organisms. Phys Scr. 2014;89(9):098003.

104. Mass T, Drake JL, Haramaty L, Kim JD, Zelzion E, Bhattacharya D, et al. Cloning and Characterization of Four Novel Coral Acid-Rich Proteins that Precipitate Carbonates In Vitro. Curr Biol. 2013 Jun 17;23(12):1126–31. doi: 10.1016/j.cub.2013.05.007 23746634

105. Mass T, Giuffre AJ, Sun C-Y, Stifler CA, Frazier MJ, Neder M, et al. Amorphous calcium carbonate particles form coral skeletons. Proc Natl Acad Sci. 2017 Aug 28;201707890.

106. Lewis B, Diaz-Pulido G. Suitability of three fluorochrome markers for obtaining in situ growth rates of coralline algae. J Exp Mar Biol Ecol. 2017 May 1;490:64–73.

107. Wegst UGK, Bai H, Saiz E, Tomsia AP, Ritchie RO. Bioinspired structural materials. Nat Mater. 2015 Jan;14(1):23–36. doi: 10.1038/nmat4089 25344782

108. van de Locht R, Slater TJA, Verch A, Young JR, Haigh SJ, Kröger R. Ultrastructure and Crystallography of Nanoscale Calcite Building Blocks in Rhabdosphaera clavigera Coccolith Spines. Cryst Growth Des. 2014 Apr 2;14(4):1710–8.

109. Leung JYS, Russell BD, Connell SD. Mineralogical Plasticity Acts as a Compensatory Mechanism to the Impacts of Ocean Acidification. Environ Sci Technol. 2017 Mar 7;51(5):2652–9. doi: 10.1021/acs.est.6b04709 28198181

110. Belcher AM, Wu XH, Christensen RJ, Hansma PK, Stucky GD, Morse DE. Control of crystal phase switching and orientation by soluble mollusc-shell proteins. Nature. 1996 May 2;381(6577):56–8.

111. Donald HK, Ries JB, Stewart JA, Fowell SE, Foster GL. Boron isotope sensitivity to seawater pH change in a species of Neogoniolithon coralline red alga. Geochim Cosmochim Acta [Internet]. 2017; Available from: http://www.sciencedirect.com/science/article/pii/S0016703717305021

112. Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, et al. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature. 2005 Sep 29;437(7059):681–6. doi: 10.1038/nature04095 16193043

113. Nash MC, Opdyke BN, Troitzsch U, Russell BD, Adey WH, Kato A, et al. Dolomite-rich coralline algae in reefs resist dissolution in acidified conditions. Nat Clim Change. 2013 Mar;3(3):268–72.

114. Cornwall CE, Hepburn CD, McGraw CM, Currie KI, Pilditch CA, Hunter KA, et al. Diurnal fluctuations in seawater pH influence the response of a calcifying macroalga to ocean acidification. Proc R Soc Lond B Biol Sci. 2013 Dec 7;280(1772):20132201.

115. Cornwall CE, Revill AT, Hurd CL. High prevalence of diffusive uptake of CO2 by macroalgae in a temperate subtidal ecosystem. Photosynth Res. 2015 May 1;124(2):181–90. doi: 10.1007/s11120-015-0114-0 25739900

116. de Carvalho RT, Salgado LT, Amado Filho GM, Leal RN, Werckmann J, Rossi AL, et al. Biomineralization of calcium carbonate in the cell wall of Lithothamnion crispatum (Hapalidiales, Rhodophyta): correlation between the organic matrix and the mineral phase. J Phycol. 2017 Mar 1;n/a–n/a.

117. Hernández-Carmona G, Hernández-Garibay E.Conventional and alternative technologies for the extraction of algal polysaccharides. Woodhead Publishing Limited,; 2013.

118. Ragazzola F, Foster LC, Jones CJ, Scott TB, Fietzke J, Kilburn MR, et al. Impact of high CO2 on the geochemistry of the coralline algae Lithothamnion glaciale. Sci Rep [Internet]. 2016 Feb 8 [cited 2017 Mar 11];6. Available from: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4744931/

119. Nash MC, Opdyke BN, Wu Z, Xu H, Trafford JM. Simple X-Ray Diffraction Techniques To Identify MG Calcite, Dolomite, and Magnesite In Tropical Coralline Algae and Assess Peak Asymmetry. J Sediment Res. 2013 Dec 1;83(12):1085–99.

120. Kata A, Baba M, Suda S. Revisions of the Mastophoroideae (corallinales, Rhodophyta) and Polyphyly in Nongeniculate Species Widely Distributed on Pacific Coral Reefs. J Phycol. 2011;47(3):662–72. doi: 10.1111/j.1529-8817.2011.00996.x 27021995

Coralline algal calcification: A morphological and process-based understanding

Souhrn

Research purpose and findings

Model for calcification

Klíčová slova:

Zdroje

PLOS One

Získaná hemofilie - Povědomí o nemoci a její diagnostika

Eozinofilní granulomatóza s polyangiitidou