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Title: Metaproteomics of a gutless marine worm and its symbiotic microbial community reveal unusual pathways for carbon and energy use

Abstract

Low nutrient and energy availability has led to the evolution of numerous strategies for overcoming these limitations, of which symbiotic associations represent a key mechanism. Particularly striking are the associations between chemosynthetic bacteria and marine animals that thrive in nutrient-poor environments such as the deep-sea because the symbionts allow their hosts to grow on inorganic energy and carbon sources such as sulfide and CO2. Remarkably little is known about the physiological strategies that enable chemosynthetic symbioses to colonize oligotrophic environments. In this study, we used metaproteomics and metabolomics to investigate the intricate network of metabolic interactions in the chemosynthetic association between Olavius algarvensis, a gutless marine worm, and its bacterial symbionts. We propose novel pathways for coping with energy and nutrient limitation, some of which may be widespread in both free-living and symbiotic bacteria. These include (i) a pathway for symbiont assimilation of the host waste products acetate, propionate, succinate and malate, (ii) the potential use of carbon monoxide as an energy source, a substrate previously not known to play a role in marine invertebrate symbioses, (iii) the potential use of hydrogen as an energy source, (iv) the strong expression of high affinity uptake transporters, and (v) novel energy efficientmore » steps in CO2 fixation and sulfate reduction. The high expression of proteins involved in pathways for energy and carbon uptake and conservation in the O. algarvensis symbiosis indicates that the oligotrophic nature of its environment exerted a strong selective pressure in shaping these associations.« less

Authors:
 [1];  [1];  [1];  [1];  [1];  [2];  [3];  [2];  [2];  [4];  [4];  [5];  [6]
  1. Max Planck Institute for Marine Microbiology
  2. ORNL
  3. Oak Ridge National Laboratory (ORNL)
  4. University of Freiburg, Germany
  5. Institute of Marine Biotechnology, Germany
  6. Institute for Microbiology, Germany
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1041080
DOE Contract Number:  
DE-AC05-00OR22725
Resource Type:
Journal Article
Journal Name:
Proceedings of the National Academy of Sciences
Additional Journal Information:
Journal Volume: 109; Journal Issue: 19; Journal ID: ISSN 0027-8424
Country of Publication:
United States
Language:
English
Subject:
08 HYDROGEN; AFFINITY; ANIMALS; AVAILABILITY; BACTERIA; CARBON; CARBON MONOXIDE; CARBON SOURCES; ENERGY SOURCES; HYDROGEN; INVERTEBRATES; NUTRIENTS; PROTEINS; SUBSTRATES; SULFATES; SULFIDES; SYMBIOSIS; WASTES; : proton translocating pyrophosphatase; pyrophosphate dependent phosphofructokinase; metaproteome; symbiosis; carbon monoxide dehydrogenase; hydrogenase; sulfate reduction; sulfide oxidation; sulfur oxidation; gutless oligochaete; Olavius algarvensis; 3-hy

Citation Formats

Kleiner, Manuel, Wentrop, C., Lott, C., Teeling, Hanno, Wetzel, Silke, Young, Jacque C, Chang, Y., Shah, Manesh B, Verberkmoes, Nathan C, Zarzycki, Jan, Fuchs, Georg, Markert, Stephanie, and Hempel, Kristina. Metaproteomics of a gutless marine worm and its symbiotic microbial community reveal unusual pathways for carbon and energy use. United States: N. p., 2012. Web. doi:10.1073/pnas.1121198109.
Kleiner, Manuel, Wentrop, C., Lott, C., Teeling, Hanno, Wetzel, Silke, Young, Jacque C, Chang, Y., Shah, Manesh B, Verberkmoes, Nathan C, Zarzycki, Jan, Fuchs, Georg, Markert, Stephanie, & Hempel, Kristina. Metaproteomics of a gutless marine worm and its symbiotic microbial community reveal unusual pathways for carbon and energy use. United States. doi:10.1073/pnas.1121198109.
Kleiner, Manuel, Wentrop, C., Lott, C., Teeling, Hanno, Wetzel, Silke, Young, Jacque C, Chang, Y., Shah, Manesh B, Verberkmoes, Nathan C, Zarzycki, Jan, Fuchs, Georg, Markert, Stephanie, and Hempel, Kristina. Sun . "Metaproteomics of a gutless marine worm and its symbiotic microbial community reveal unusual pathways for carbon and energy use". United States. doi:10.1073/pnas.1121198109.
@article{osti_1041080,
title = {Metaproteomics of a gutless marine worm and its symbiotic microbial community reveal unusual pathways for carbon and energy use},
author = {Kleiner, Manuel and Wentrop, C. and Lott, C. and Teeling, Hanno and Wetzel, Silke and Young, Jacque C and Chang, Y. and Shah, Manesh B and Verberkmoes, Nathan C and Zarzycki, Jan and Fuchs, Georg and Markert, Stephanie and Hempel, Kristina},
abstractNote = {Low nutrient and energy availability has led to the evolution of numerous strategies for overcoming these limitations, of which symbiotic associations represent a key mechanism. Particularly striking are the associations between chemosynthetic bacteria and marine animals that thrive in nutrient-poor environments such as the deep-sea because the symbionts allow their hosts to grow on inorganic energy and carbon sources such as sulfide and CO2. Remarkably little is known about the physiological strategies that enable chemosynthetic symbioses to colonize oligotrophic environments. In this study, we used metaproteomics and metabolomics to investigate the intricate network of metabolic interactions in the chemosynthetic association between Olavius algarvensis, a gutless marine worm, and its bacterial symbionts. We propose novel pathways for coping with energy and nutrient limitation, some of which may be widespread in both free-living and symbiotic bacteria. These include (i) a pathway for symbiont assimilation of the host waste products acetate, propionate, succinate and malate, (ii) the potential use of carbon monoxide as an energy source, a substrate previously not known to play a role in marine invertebrate symbioses, (iii) the potential use of hydrogen as an energy source, (iv) the strong expression of high affinity uptake transporters, and (v) novel energy efficient steps in CO2 fixation and sulfate reduction. The high expression of proteins involved in pathways for energy and carbon uptake and conservation in the O. algarvensis symbiosis indicates that the oligotrophic nature of its environment exerted a strong selective pressure in shaping these associations.},
doi = {10.1073/pnas.1121198109},
journal = {Proceedings of the National Academy of Sciences},
issn = {0027-8424},
number = 19,
volume = 109,
place = {United States},
year = {2012},
month = {1}
}