Coral host cells acidify symbiotic algal microenvironment to promote photosynthesis

被引:145
作者
Barott, Katie L. [1 ]
Venn, Alexander A. [2 ,3 ]
Perez, Sidney O. [1 ]
Tambutte, Sylvie [2 ]
Tresguerres, Martin [1 ]
机构
[1] Univ Calif San Diego, Scripps Inst Oceanog, Marine Biol Res Div, La Jolla, CA 92093 USA
[2] Ctr Sci Monaco, Dept Marine Biol, MC-98000 Monaco, Monaco
[3] Ctr Sci Monaco, CNRS, Lab Europeen Associe Biosensib 647, MC-98000 Monaco, Monaco
基金
美国国家科学基金会;
关键词
proton pump; V type H+ ATPase; zooxanthellae; Symbiodinium; carbon concentrating mechanism; INORGANIC CARBON UPTAKE; INTRACELLULAR PH; H+-ATPASE; DINOFLAGELLATE ASSOCIATION; AMMONIA EXCRETION; ORGANIC MATRIX; MECHANISMS; BICARBONATE; TRANSPORT; ANEMONE;
D O I
10.1073/pnas.1413483112
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Symbiotic dinoflagellate algae residing inside coral tissues supply the host with the majority of their energy requirements through the translocation of photosynthetically fixed carbon. The algae, in turn, rely on the host for the supply of inorganic carbon. Carbon must be concentrated as CO2 in order for photosynthesis to proceed, and here we show that the coral host plays an active role in this process. The host-derived symbiosome membrane surrounding the algae abundantly expresses vacuolar H+-ATPase (VHA), which acidifies the symbiosome space down to pH similar to 4. Inhibition of VHA results in a significant decrease in average H+ activity in the symbiosome of up to 75% and a significant reduction in O-2 production rate, a measure of photosynthetic activity. These results suggest that host VHA is part of a previously unidentified carbon concentrating mechanism for algal photosynthesis and provide mechanistic evidence that coral host cells can actively modulate the physiology of their symbionts.
引用
收藏
页码:607 / 612
页数:6
相关论文
共 46 条
[11]   Ammonia and amino acid transport across symbiotic membranes in nitrogen-fixing legume nodules [J].
Day, DA ;
Poole, PS ;
Tyerman, SD ;
Rosendahl, L .
CELLULAR AND MOLECULAR LIFE SCIENCES, 2001, 58 (01) :61-71
[12]   Localization of H+ -ATPase in soybean root nodules [J].
Fedorova, E ;
Thomson, R ;
Whitehead, LF ;
Maudoux, O ;
Udvardi, MK ;
Day, DA .
PLANTA, 1999, 209 (01) :25-32
[13]   Intracellular pH of symbiotic dinoflagellates [J].
Gibbin, E. M. ;
Davy, S. K. .
CORAL REEFS, 2013, 32 (03) :859-863
[14]   Intracellular pH and its response to CO2-driven seawater acidification in symbiotic versus non-symbiotic coral cells [J].
Gibbin, Emma M. ;
Putnam, Hollie M. ;
Davy, Simon K. ;
Gates, Ruth D. .
JOURNAL OF EXPERIMENTAL BIOLOGY, 2014, 217 (11) :1963-1969
[15]   Inorganic carbon uptake for photosynthesis by the symbiotic coral/dinoflagellate association .1. Photosynthetic performances of symbionts and dependence on sea water bicarbonate [J].
Goiran, C ;
AlMoghrabi, S ;
Allemand, D ;
Jaubert, J .
JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY, 1996, 199 (02) :207-225
[16]   The reef coral two compartment proton flux model: A new approach relating tissue-level physiological processes to gross corallum morphology [J].
Jokiel, Paul L. .
JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY, 2011, 409 (1-2) :1-12
[17]   Major Cellular and Physiological Impacts of Ocean Acidification on a Reef Building Coral [J].
Kaniewska, Paulina ;
Campbell, Paul R. ;
Kline, David I. ;
Rodriguez-Lanetty, Mauricio ;
Miller, David J. ;
Dove, Sophie ;
Hoegh-Guldberg, Ove .
PLOS ONE, 2012, 7 (04)
[18]   Transcriptome Analysis of the Scleractinian Coral Stylophora pistillata [J].
Karako-Lampert, Sarit ;
Zoccola, Didier ;
Salmon-Divon, Mali ;
Katzenellenbogen, Mark ;
Tambutte, Sylvie ;
Bertucci, Anthony ;
Hoegh-Guldberg, Ove ;
Deleury, Emeline ;
Allemand, Denis ;
Levy, Oren .
PLOS ONE, 2014, 9 (02)
[19]  
Knowlton Nancy, 2010, P65, DOI 10.1002/9781444325508.ch4
[20]  
Laurent J, 2012, J EXP BIOL