Microenvironmental changes support evidence of photosynthesis and calcification inhibition in Halimeda under ocean acidification and warming
详细信息 查看全文
- 作者：S. Sinutok (1)
R. Hill (1) (4)
M. A. Doblin (1)
M. Kühl (1) (2) (3)
P. J. Ralph (1) - 关键词：Chlorophyll fluorescence ; Climate change ; Microsensor ; Macroalgae ; Coral reefs
- 刊名：Coral Reefs
- 出版年：2012
- 出版时间：December 2012
- 年：2012
- 卷：31
- 期：4
- 页码：1201-1213
- 全文大小：891KB
- 参考文献：1. Al-Horani FA (2005) Effects of changing seawater temperature on photosynthesis and calcification in the scleractinian coral / Galaxea fascicularis, measured with O<sub class="a-plus-plus">2sub>, Ca<sup class="a-plus-plus">2+sup> and pH microsensors. Sci Mar 69:347-54 ss="external" href="http://dx.doi.org/10.3989/scimar.2005.69n3347">CrossRef
2. Allakhverdiev SI, Kreslavski VD, Klimov VV, Los DA, Carpentier R, Mohanty P (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res 98:541-50 ss="external" href="http://dx.doi.org/10.1007/s11120-008-9331-0">CrossRef
3. Anthony KRN, Kline DI, Diaz-Pulido G, Dove S, Hoegh-Guldberg O (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc Natl Acad Sci USA 105:17442-7446 ss="external" href="http://dx.doi.org/10.1073/pnas.0804478105">CrossRef
4. Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Physiol 59:89-13
5. Blaxter JHS, Russel FS, Young M (eds) (1980) Ecology and taxonomy of / Halimeda: primary producer of coral reefs. Academic Press, New York
6. Borowitzka MA (1977) Algal calcification. Oceanogr Mar Biol Annu Rev 15:189-23
7. Borowitzka MA (1986) Physiology and biochemistry of calcification in the Chlorophyceae. In: Leadbeater B, Riding H (eds) Biomineralization in the lower plants and animals. Oxford University Press, Oxford, pp 107-24
8. Borowitzka MA (1989) Carbonate calcification in algae—initiation and control. In: Mann S, Webb J, Williams RJP (eds) Biomineralization: Chemical and biochemical perspectives. VCH, Weinheim, pp 63-4
9. Borowitzka MA, Larkum AWD (1976a) Calcification in the green alga / Halimeda II. The exchange of Ca<sup class="a-plus-plus">2+sup> and the occurrence of age gradients in calcification and photosynthesis. J Exp Bot 27:864-78 ss="external" href="http://dx.doi.org/10.1093/jxb/27.5.864">CrossRef
10. Borowitzka MA, Larkum AWD (1976b) Calcification in the green alga / Halimeda III. The sources of inorganic carbon for photosynthesis and calcification and a model of the mechanism of calcification. J Exp Bot 27:879-93 ss="external" href="http://dx.doi.org/10.1093/jxb/27.5.879">CrossRef
11. Borowitzka MA, Larkum AWD (1977) Calcification in the green alga / Halimeda. I. An ultrastructure study on thallus development. J Phycol 13:6-6
12. Borowitzka MA, Larkum AWD, Nockolds CE (1974) A scanning electron microscope study of the structure and organization of the calcium carbonate deposits of algae. Phycologia 13:195-03 ss="external" href="http://dx.doi.org/10.2216/i0031-8884-13-3-195.1">CrossRef
13. De Beer D, Larkum AWD (2001) Photosynthesis and calcification in the calcifying algae / Halimeda discoidea studied with microsensors. Plant, Cell Environ 24:1209-217 ss="external" href="http://dx.doi.org/10.1046/j.1365-3040.2001.00772.x">CrossRef
14. Diaz-Pulido G, McCook LJ, Larkum AWD, Lotze HK, Raven JA, Schaffelke B, Smith JE, Steneck RS (2007) Vulnerability of macroalgae of the Great Barrier Reef to climate change. In: Johnson JE, Marshall PA (eds) Climate change and the Great Barrier Reef. Great Barrier Reef Marine Park Authority and Australian Greenhouse Office, Australia, pp 153-92
15. Drew EA (1983) / Halimeda biomass, growth rates and sediment generation on reefs in the Central Great Barrier Reef Province. Coral Reefs 2:101-10 ss="external" href="http://dx.doi.org/10.1007/BF02395280">CrossRef
16. Feely RA, Sabine CL, Lee K, Berelson W, Kleypas J, Fabry VJ, Millero FJ (2004) Impact of anthropogenic CO<sub class="a-plus-plus">2sub> on the CaCO<sub class="a-plus-plus">3sub> system in the oceans. Science 305:362-66 ss="external" href="http://dx.doi.org/10.1126/science.1097329">CrossRef
17. Fujita K, Hikami M, Suzuki A, Kuroyanagi A, Sakai K, Kawahata H, Nojiri Y (2011) Effects of ocean acidification on calcification of symbiont-bearing reef foraminifers. Biogeosciences 8:2089-098 ss="external" href="http://dx.doi.org/10.5194/bg-8-2089-2011">CrossRef
18. Gao K, Aruga Y, Asada K, Kiyohara M (1993) Influence of enhanced CO<sub class="a-plus-plus">2sub> on growth and photosynthesis of the red algae / Gracilaria sp. and / G. chilensis. J Appl Phycol 5:563-71 ss="external" href="http://dx.doi.org/10.1007/BF02184635">CrossRef
19. Gattuso J-P, Lavigne H (2009) Technical note: approaches and software tools to investigate the impact of ocean acidification. Biogeosciences 6:2121-133 ss="external" href="http://dx.doi.org/10.5194/bg-6-2121-2009">CrossRef
20. Glud RN, Gundersen JK, Revsbech NP, J?rgensen BB (1995) Effects on the benthic diffusive boundary layer imposed by microelectrodes. Limnol Oceanogr 39:462-67 ss="external" href="http://dx.doi.org/10.4319/lo.1994.39.2.0462">CrossRef
21. Guinotte JM, Buddemeier RW, Kleypas JA (2003) Future coral reef habitat marginality: temporal and spatial effects of climate change in the Pacific basin. Coral Reefs 22:551-58 ss="external" href="http://dx.doi.org/10.1007/s00338-003-0331-4">CrossRef
22. Hall-Spencer JM, Rodolfo-Metalpa R, Martin S, Ransome E, Fine M, Turner SM, Rowley SJ, Tedesco D, Buia M-C (2008) Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454:96-9 ss="external" href="http://dx.doi.org/10.1038/nature07051">CrossRef
23. Hill R, Larkum AWD, Frankart C, Kühl M, Ralph PJ (2004) Loss of functional photosystem II reaction centres in zooxanthellae of corals exposed to bleaching conditions: using fluorescence rise kinetics. Photosynth Res 82:59-2 ss="external" href="http://dx.doi.org/10.1023/B:PRES.0000040444.41179.09">CrossRef
24. Hofmann LC, Yildiz G, Hanelt D, Bischof K (2012) Physiological responses of the calcifying rhodophyte, / Corallina officinalis (L.), to future CO<sub class="a-plus-plus">2sub> levels. Mar Biol 159:783-92 ss="external" href="http://dx.doi.org/10.1007/s00227-011-1854-9">CrossRef
25. Houghton J (2009) Global warming: the complete briefing. Cambridge University Press, United Kingdom ss="external" href="http://dx.doi.org/10.1017/CBO9780511841590">CrossRef
26. Iglesias-Prieto R, Beltrán VH, LaJeunesse TC, Reyes-Bonilla H, Thome PE (2004) Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proc R Soc Biol Sci Ser B 271:1757-763 ss="external" href="http://dx.doi.org/10.1098/rspb.2004.2757">CrossRef
27. Jokiel PL, Maracios JE, Franzisket L (eds) (1978) Coral growth: buoyant weight technique. In: Stoddart DR, Johannes RE (eds) Coral reefs: Research methods, UNESCO, pp 529-41
28. Jokiel PL, Rodgers KS, Kuffner IB, Andersson AJ, Cox EF, Mackenzie FT (2008) Ocean acidification and calcifying reef organisms: a mesocosm investigation. Coral Reefs 27:473-83 ss="external" href="http://dx.doi.org/10.1007/s00338-008-0380-9">CrossRef
29. Kleypas JA, Yates KK (2009) Coral reefs and ocean acidification. Oceanography 22:108-17 ss="external" href="http://dx.doi.org/10.5670/oceanog.2009.101">CrossRef
30. Kleypas JA, Buddemeier RW, Archer D, Gattuso J-P, Langdon C, Opdyke BN (1999) Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science 284:118-20 ss="external" href="http://dx.doi.org/10.1126/science.284.5411.118">CrossRef
31. K?hler-Rink S, Kühl M (2000) Microsensor studies of photosynthesis and respiration in larger symbiotic foraminifera. I The physio-chemical microenvironment of / Marginopora vertebralis, / Amphistegina lobifera and / Amphisorus hemprichii. Mar Biol 137:473-86 ss="external" href="http://dx.doi.org/10.1007/s002270000335">CrossRef
32. K?hler-Rink S, Kühl M (2005) The chemical microenvironment of the symbiotic planktonic foraminifer / Orbulina universa. Mar Biol Res 1:68-8 ss="external" href="http://dx.doi.org/10.1080/17451000510019015">CrossRef
33. Kuffner IB, Andersson AJ, Jokiel PL, Rodgers KS, Mackenzie FT (2007) Decreased abundance of crustose coralline algae due to ocean acidification. Nat Geosci 1:114-17 ss="external" href="http://dx.doi.org/10.1038/ngeo100">CrossRef
34. Kuguru B, Achituv Y, Gruber DF, Tchernov D (2010) Photoacclimation mechanisms of corallimorpharians on coral reefs: photosynthetic parameters of zooxanthellae and host cellular responses to variation in irradiance. J Exp Mar Biol Ecol 394:53-2 ss="external" href="http://dx.doi.org/10.1016/j.jembe.2010.07.007">CrossRef
35. Langdon C, Gattuso J-P, Anderson A (2010) Measurements of calcification and dissolution of benthic organisms and communities. In: Riebesell U, Fabry VJ, Hansson L, Gattuso J-P (eds) Guide to best practices for ocean acidification research and data reporting. Publication Office of the European Union, Luxembourg, pp 213-32
36. Larkum AWD, Salih A, Kühl M (2011) Rapid mass movement of chloroplasts during segment formation of the calcifying siphonalean green alga / Halimeda macroloba. PLoS One 6. doi:<span class="a-plus-plus non-url-ref">10.1371/journal.pone.0020841
37. Lewis E, Wallace DWR (1998) CO2SYS—Program developed for the CO2 system calculations. Carbon Dioxide Information Analysis Center; Report ORNL/CDIAC-105, Oakridge National Laboratory, Oakridge, TN
38. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659-68 ss="external" href="http://dx.doi.org/10.1093/jexbot/51.345.659">CrossRef
39. McConnaughey T (1989) Biomineralization mechanisms. In: Crick RE (ed) Origin, evolution, and modern aspects of biomineralization in plants and animals. Plenum Press, New York, pp 57-3
40. McConnaughey TA, Whelan JF (1997) Calcification generates protons for nutrient and bicarbonate uptake. Earth-Sci Rev 42:95-17 ss="external" href="http://dx.doi.org/10.1016/S0012-8252(96)00036-0">CrossRef
41. Palacios SL, Zimmerman RC (2007) Response of eelgrass / Zostera marina to CO<sub class="a-plus-plus">2sub> enrichment: possible impacts of climate change and potential for remediation of coastal habitats. Mar Ecol Prog Ser 344:1-3 ss="external" href="http://dx.doi.org/10.3354/meps07084">CrossRef
42. Revsbech NP, Jorgensen BB, Brix O (1981) Primary production of microalgae in sediments measured by oxygen microprofile, H<sup class="a-plus-plus">14sup>CO<sub class="a-plus-plus">3sub> <sup class="a-plus-plus">?/sup> fixation, and oxygen exchange methods. Limnol Oceanogr 26:717-30 ss="external" href="http://dx.doi.org/10.4319/lo.1981.26.4.0717">CrossRef
43. Ries JB (2011) A physicochemical framework for interpreting the biological calcification response to CO<sub class="a-plus-plus">2sub>-induced ocean acidification. Geochim Cosmochim Acta 75:4053-064 ss="external" href="http://dx.doi.org/10.1016/j.gca.2011.04.025">CrossRef
44. Ritchie RJ (2008) Universal chlorophyll equations for estimating chlorophylls / a, b, c, and / d and total chlorophylls in natural assemblages of photosynthetic organisms using acetone, methanol, or ethanol solvents. Photosynthetica 46:115-26 ss="external" href="http://dx.doi.org/10.1007/s11099-008-0019-7">CrossRef
45. Schreiber U (2004) Pulse-amplitude-modulation (PAM) fluorometry and saturation pulse method: An overview. In: Papageorgiou GC, Govindjee (eds) Chlorophyll / a fluorescence: A signature of photosynthesis. Springer, Dordrecht, pp 279-19
46. Short FT, Neckles HA (1999) The effects of global climate change on seagrasses. Aquat Bot 63:169-96 ss="external" href="http://dx.doi.org/10.1016/S0304-3770(98)00117-X">CrossRef
47. Sinutok S, Hill R, Doblin MA, Wuhrer R, Ralph PJ (2011) Warmer more acidic conditions cause decreased productivity and calcification in subtropical coral reef sediment-dwelling calcifiers. Limnol Oceanogr 56:1200-212 ss="external" href="http://dx.doi.org/10.4319/lo.2011.56.4.1200">CrossRef
48. Smith SV, Kinsey DW (1976) Calcium carbonate production, coral reef growth, and sea level change. Science 194:937-39 ss="external" href="http://dx.doi.org/10.1126/science.194.4268.937">CrossRef
49. Warner ME, Fitt WK, Schimidt GW (1999) Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc Natl Acad Sci USA 96:8007-012 ss="external" href="http://dx.doi.org/10.1073/pnas.96.14.8007">CrossRef
50. Weyl PK (1959) The change in solubility of calcium carbonate with temperature and carbon dioxide content. Geochim Cosmochim Acta 17:214-25 ss="external" href="http://dx.doi.org/10.1016/0016-7037(59)90096-1">CrossRef - 作者单位：S. Sinutok (1)
R. Hill (1) (4)
M. A. Doblin (1)
M. Kühl (1) (2) (3)
P. J. Ralph (1)
1. Plant Functional Biology and Climate Change Cluster, School of the Environment, University of Technology Sydney, PO Box 123, Broadway, Sydney, NSW, 2007, Australia
4. Centre for Marine Bio-Innovation and Sydney Institute of Marine Science, School of Biological, Earth and Environmental Sciences, The University of New South Wales, Sydney, NSW, 2052, Australia
2. Marine Biology Section, Department of Biology, University of Copenhagen, Strandpromenaden 5, 3000, Helsing?r, Denmark
3. Singapore Centre on Environmental Life Sciences Engineering, School of Biological Sciences, Nanyang Technological University, Nanyang Avenue, Singapore - ISSN：1432-0975
文摘
The effects of elevated CO2sub> and temperature on photosynthesis and calcification of two important calcifying reef algae (Halimeda macroloba and Halimeda cylindracea) were investigated with O2sub> microsensors and chlorophyll a fluorometry through a combination of two pCO2sub> (400 and 1,200?μatm) and two temperature treatments (28 and 32?°C) equivalent to the present and predicted conditions during the 2100 austral summer. Combined exposure to pCO2sub> and elevated temperature impaired calcification and photosynthesis in the two Halimeda species due to changes in the microenvironment around the algal segments and a reduction in physiological performance. There were no significant changes in controls over the 5-week experiment, but there was a 50-0?% decrease in photochemical efficiency (maximum quantum yield), a 70-0?% decrease in O2sub> production and a threefold reduction in calcification rate in the elevated CO2sub> and high temperature treatment. Calcification in these species is closely coupled with photosynthesis, such that a decrease in photosynthetic efficiency leads to a decrease in calcification. Although pH seems to be the main factor affecting Halimeda species, heat stress also has an impact on their photosystem II photochemical efficiency. There was a strong combined effect of elevated CO2sub> and temperature in both species, where exposure to elevated CO2sub> or temperature alone decreased photosynthesis and calcification, but exposure to both elevated CO2sub> and temperature caused a greater decline in photosynthesis and calcification than in each stress individually. Our study shows that ocean acidification and ocean warming are drivers of calcification and photosynthesis inhibition in Halimeda. Predicted climate change scenarios for 2100 would therefore severely affect the fitness of Halimeda, which can result in a strongly reduced production of carbonate sediments on coral reefs under such changed climate conditions.