Use of carbon monoxide and hydrogen by a bacteria-animal symbiosis from seagrass sediments

Environ Microbiol. 2015 Dec;17(12):5023-35. doi: 10.1111/1462-2920.12912. Epub 2015 Jul 23.

Abstract

The gutless marine worm Olavius algarvensis lives in symbiosis with chemosynthetic bacteria that provide nutrition by fixing carbon dioxide (CO2 ) into biomass using reduced sulfur compounds as energy sources. A recent metaproteomic analysis of the O. algarvensis symbiosis indicated that carbon monoxide (CO) and hydrogen (H2 ) might also be used as energy sources. We provide direct evidence that the O. algarvensis symbiosis consumes CO and H2 . Single cell imaging using nanoscale secondary ion mass spectrometry revealed that one of the symbionts, the γ3-symbiont, uses the energy from CO oxidation to fix CO2 . Pore water analysis revealed considerable in-situ concentrations of CO and H2 in the O. algarvensis environment, Mediterranean seagrass sediments. Pore water H2 concentrations (89-2147 nM) were up to two orders of magnitude higher than in seawater, and up to 36-fold higher than previously known from shallow-water marine sediments. Pore water CO concentrations (17-51 nM) were twice as high as in the overlying seawater (no literature data from other shallow-water sediments are available for comparison). Ex-situ incubation experiments showed that dead seagrass rhizomes produced large amounts of CO. CO production from decaying plant material could thus be a significant energy source for microbial primary production in seagrass sediments.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bacteria / metabolism*
  • Carbon Dioxide / metabolism
  • Carbon Monoxide / metabolism*
  • Energy Metabolism
  • Geologic Sediments / microbiology*
  • Hydrogen / metabolism*
  • Mediterranean Region
  • Oligochaeta / microbiology*
  • Oxidation-Reduction
  • Seawater / microbiology*
  • Spectrometry, Mass, Secondary Ion
  • Sulfur Compounds / metabolism
  • Symbiosis

Substances

  • Sulfur Compounds
  • Carbon Dioxide
  • Carbon Monoxide
  • Hydrogen