A novel symbiosis between chemoautotrophic bacteria and a freshwater cave amphipod

Sharmishtha Dattagupta, Irene Schaperdoth, Alessandro Montanari, Sandro Mariani, Noriko Kita, John W. Valley, Jennifer Macalady

Research output: Contribution to journalArticle

60 Citations (Scopus)

Abstract

Symbioses involving animals and chemoautotrophic bacteria form the foundation of entire ecosystems at deep-sea hydrothermal vents and cold seeps, but have so far not been reported in terrestrial or freshwater environments. A rare example of a terrestrial ecosystem sustained by chemoautotrophy is found within the sulfide-rich Frasassi limestone cave complex of central Italy. In this study, we report the discovery of abundant filamentous bacteria on the exoskeleton of Niphargus ictus, a macroinvertebrate endemic to Frasassi. Using 16S rDNA sequencing and fluorescence in situ hybridization (FISH), we show that N. ictus throughout the large cave complex are colonized by a single phylotype of bacteria in the sulfur-oxidizing clade Thiothrix. The epibiont phylotype is distinct from Thiothrix phylotypes that form conspicuous biofilms in the cave streams and pools inhabited by N. ictus. Using a combination of 13 C labeling, FISH, and secondary ion mass spectrometry (SIMS), we show that the epibiotic Thiothrix are autotrophic, establishing the first known example of a non-marine chemoautotroph-animal symbiosis. Conditions supporting chemoautotrophy, and the N. ictus-Thiothrix association, likely commenced in the Frasassi cave complex between 350 000 and 1 million years ago. Therefore, the N. ictus-Thiothrix symbiosis is probably significantly younger than marine chemoautotrophic symbioses, many of which have been evolving for tens to hundreds of million years.

Original languageEnglish (US)
Pages (from-to)935-943
Number of pages9
JournalISME Journal
Volume3
Issue number8
DOIs
StatePublished - Aug 1 2009

Fingerprint

Thiothrix
Amphipoda
Symbiosis
symbiosis
Fresh Water
caves
amphipod
cave
chemoautotrophy
Chemoautotrophic Growth
Bacteria
bacterium
Hydrothermal Vents
bacteria
fluorescence in situ hybridization
Fluorescence In Situ Hybridization
fluorescence
Ecosystem
epibiont
cold seep

All Science Journal Classification (ASJC) codes

  • Microbiology
  • Ecology, Evolution, Behavior and Systematics

Cite this

Dattagupta, Sharmishtha ; Schaperdoth, Irene ; Montanari, Alessandro ; Mariani, Sandro ; Kita, Noriko ; Valley, John W. ; Macalady, Jennifer. / A novel symbiosis between chemoautotrophic bacteria and a freshwater cave amphipod. In: ISME Journal. 2009 ; Vol. 3, No. 8. pp. 935-943.
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A novel symbiosis between chemoautotrophic bacteria and a freshwater cave amphipod. / Dattagupta, Sharmishtha; Schaperdoth, Irene; Montanari, Alessandro; Mariani, Sandro; Kita, Noriko; Valley, John W.; Macalady, Jennifer.

In: ISME Journal, Vol. 3, No. 8, 01.08.2009, p. 935-943.

Research output: Contribution to journalArticle

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