The fingerprint of chemosymbiosis: origin and preservation of isotopic biosignatures in the nonseep bivalve Loripes lacteus compared with Venerupis aurea

FEMS Microbiol Ecol. 2012 Aug;81(2):480-93. doi: 10.1111/j.1574-6941.2012.01374.x. Epub 2012 May 23.

Abstract

Endosymbionts in marine bivalves leave characteristic biosignatures in their host organisms. Two nonseep bivalve species collected in Mediterranean lagoons, thiotrophic symbiotic Loripes lacteus and filter-feeding nonsymbiotic Venerupis aurea, were studied in detail with respect to generation and presence of such signatures in living animals, and the preservation of these signals in subfossil (late Pleistocene) sedimentary shells. Three key enzymes from sulfur oxidation (APS-reductase), CO(2) fixation (RubisCO) and assimilation of nitrogen [glutamine synthetase (GS)] were detected by immunofluorescence in the bacterial symbionts of Loripes. In Loripes, major activity was derived from GS of the symbionts whereas in Venerupis the host GS is active. In search of geologically stable biosignatures for thiotrophic chemosymbiosis that might be suitable to detect such associations in ancient bivalves, we analyzed the isotopic composition of shell lipids (δ(13)C) and the bulk organic matrix of the shell (δ(13)C , δ(15)N , δ(34)S). In the thiotrophic Loripes, δ(13)C values were depleted compared with the filter-feeding Venerupis by as much as 8.5‰ for individual fatty acids, and 4.4‰ for bulk organic carbon. Likewise, bulk δ(15)N and δ(34)S values were more depleted in recent thiotrophic Loripes. Whereas δ (34)S values were found to be unstable over time, the combined δ(15)N and δ(13)C values in organic shell extracts revealed a specific signature for chemosymbiosis in recent and subfossil specimens.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animal Shells / chemistry*
  • Animals
  • Bacteria / enzymology*
  • Bacteria / genetics
  • Bivalvia / chemistry
  • Bivalvia / microbiology*
  • Carbon Cycle
  • Carbon Isotopes / analysis*
  • Fossils
  • Glutamate-Ammonia Ligase / analysis
  • Nitrogen / chemistry
  • Nitrogen Isotopes / analysis
  • Oxidation-Reduction
  • Oxidoreductases Acting on Sulfur Group Donors / analysis
  • RNA, Ribosomal, 16S / genetics
  • Ribulose-Bisphosphate Carboxylase / analysis
  • Sulfur / analysis
  • Sulfur Isotopes / analysis
  • Symbiosis*

Substances

  • Carbon Isotopes
  • Nitrogen Isotopes
  • RNA, Ribosomal, 16S
  • Sulfur Isotopes
  • Sulfur
  • Oxidoreductases Acting on Sulfur Group Donors
  • adenylylsulfate reductase
  • Ribulose-Bisphosphate Carboxylase
  • Glutamate-Ammonia Ligase
  • Nitrogen