Linking Hydrothermal Geochemistry to Organismal Physiology: Physiological Versatility in Riftia pachyptila from Sedimented and Basalt-hosted Vents

被引:23
作者
Robidart, Julie C. [1 ]
Roque, Annelys [2 ]
Song, Pengfei [3 ]
Girguis, Peter R. [3 ]
机构
[1] Univ Calif Santa Cruz, Dept Ocean Sci, Santa Cruz, CA 95064 USA
[2] NIH, Vaccine Res Ctr, Bethesda, MD 20892 USA
[3] Harvard Univ, Cambridge, MA 02138 USA
基金
美国国家科学基金会;
关键词
EAST PACIFIC RISE; TUBE-WORM; GUAYMAS BASIN; ROSE GARDEN; CHEMOAUTOTROPHIC SYMBIONTS; CARBONIC-ANHYDRASE; METABOLITE UPTAKE; INORGANIC CARBON; ACID CYCLE; SULFIDE;
D O I
10.1371/journal.pone.0021692
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
Much of what is known regarding Riftia pachyptila physiology is based on the wealth of studies of tubeworms living at diffuse flows along the fast-spreading, basalt-hosted East Pacific Rise (EPR). These studies have collectively suggested that Riftia pachyptila and its chemoautotrophic symbionts are physiologically specialized, highly productive associations relying on hydrogen sulfide and oxygen to generate energy for carbon fixation, and the symbiont's nitrate reduction to ammonia for energy and biosynthesis. However, Riftia also flourish in sediment-hosted vents, which are markedly different in geochemistry than basalt-hosted systems. Here we present data from shipboard physiological studies and global quantitative proteomic analyses of Riftia pachyptila trophosome tissue recovered from tubeworms residing in the EPR and the Guaymas basin, a sedimented, hydrothermal vent field. We observed marked differences in symbiont nitrogen metabolism in both the respirometric and proteomic data. The proteomic data further suggest that Riftia associations in Guaymas may utilize different sulfur compounds for energy generation, may have an increased capacity for energy storage, and may play a role in degrading exogenous organic carbon. Together these data reveal that Riftia symbionts are far more physiologically plastic than previously considered, and that contrary to previous assertions-Riftia do assimilate reduced nitrogen in some habitats. These observations raise new hypotheses regarding adaptations to the geochemical diversity of habitats occupied by Riftia, and the degree to which the environment influences symbiont physiology and evolution.
引用
收藏
页数:12
相关论文
共 75 条
[1]  
ARP AJ, 1987, J EXP BIOL, V128, P139
[2]   Structural basis for the oxidation of thiosulfate by a sulfur cycle enzyme [J].
Bamford, VA ;
Bruno, S ;
Rasmussen, T ;
Appia-Ayme, C ;
Cheesman, MR ;
Berks, BC ;
Hemmings, AM .
EMBO JOURNAL, 2002, 21 (21) :5599-5610
[3]   HYDROCARBONS IN SURFACE SEDIMENTS FROM A GUAYMAS BASIN HYDROTHERMAL VENT SITE [J].
BAZYLINSKI, DA ;
FARRINGTON, JW ;
JANNASCH, HW .
ORGANIC GEOCHEMISTRY, 1988, 12 (06) :547-558
[4]   ENZYMES OF THE REDUCTIVE CITRIC-ACID CYCLE IN THE AUTOTROPHIC EUBACTERIUM AQUIFEX-PYROPHILUS AND IN THE ARCHAEBACTERIUM THERMOPROTEUS-NEUTROPHILUS [J].
BEH, M ;
STRAUSS, G ;
HUBER, R ;
STETTER, KO ;
FUCHS, G .
ARCHIVES OF MICROBIOLOGY, 1993, 160 (04) :306-311
[5]   An autoradiographic examination of carbon fixation, transfer and utilization in the Riftia pachyptila symbiosis [J].
Bright, M ;
Keckeis, H ;
Fisher, CR .
MARINE BIOLOGY, 2000, 136 (04) :621-632
[6]   A REVERSE KREBS CYCLE IN PHOTOSYNTHESIS - CONSENSUS AT LAST [J].
BUCHANAN, BB ;
ARNON, DI .
PHOTOSYNTHESIS RESEARCH, 1990, 24 (01) :47-53
[7]   Seafloor eruptions and evolution of hydrothermal fluid chemistry [J].
Butterfield, DA ;
Jonasson, IR ;
Massoth, GJ ;
Feely, RA ;
Roe, KK ;
Embley, RE ;
Holden, JF ;
McDuff, RE ;
Lilley, MD ;
Delaney, JR .
PHILOSOPHICAL TRANSACTIONS OF THE ROYAL SOCIETY A-MATHEMATICAL PHYSICAL AND ENGINEERING SCIENCES, 1997, 355 (1723) :369-386
[8]   A TIME-SERIES OF VENT FLUID COMPOSITIONS FROM 21-DEGREES-N, EAST PACIFIC RISE (1979, 1981, 1985), AND THE GUAYMAS BASIN, GULF OF CALIFORNIA (1982, 1985) [J].
CAMPBELL, AC ;
BOWERS, TS ;
MEASURES, CI ;
FALKNER, KK ;
KHADEM, M ;
EDMOND, JM .
JOURNAL OF GEOPHYSICAL RESEARCH-SOLID EARTH AND PLANETS, 1988, 93 (B5) :4537-4549
[9]   PROKARYOTIC CELLS IN THE HYDROTHERMAL VENT TUBE WORM RIFTIA-PACHYPTILA JONES - POSSIBLE CHEMOAUTOTROPHIC SYMBIONTS [J].
CAVANAUGH, CM ;
GARDINER, SL ;
JONES, ML ;
JANNASCH, HW ;
WATERBURY, JB .
SCIENCE, 1981, 213 (4505) :340-342
[10]   The metabolic demands of endosymbiotic chemoautotrophic metabolism on host physiological capacities [J].
Childress, J. J. ;
Girguis, P. R. .
JOURNAL OF EXPERIMENTAL BIOLOGY, 2011, 214 (02) :312-325