A novel symbiosis between chemoautotrophic bacteria and a freshwater cave amphipod.
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 13C 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.
Department of Geosciences, Pennsylvania State University, University Park, PA, USA. sdattag@uni-goettingen.de
Sharmishtha
S
Dattagupta
Irene
I
Schaperdoth
Alessandro
A
Montanari
Sandro
S
Mariani
Noriko
N
Kita
John W
JW
Valley
Jennifer L
JL
Macalady
D033304:Amphipoda / Q000382:microbiology* / Q000502:physiology*; D000818:Animals; D018407:Bacterial Physiological Phenomena; D016000:Cluster Analysis; D004269:DNA, Bacterial / Q000737:chemistry / Q000235:genetics; D004275:DNA, Ribosomal / Q000737:chemistry / Q000235:genetics; D005618:Fresh Water; D017404:In Situ Hybridization, Fluorescence; D007287:Inorganic Chemicals / Q000378:metabolism; D007558:Italy; D008969:Molecular Sequence Data; D010802:Phylogeny; D012336:RNA, Ribosomal, 16S / Q000235:genetics; D017422:Sequence Analysis, DNA; D013559:Symbiosis; D053525:Thiothrix / Q000145:classification* / Q000235:genetics / Q000302:isolation & purification* / Q000378:metabolism
D004269:DNA, Bacterial; D004275:DNA, Ribosomal; D007287:Inorganic Chemicals; D012336:RNA, Ribosomal, 16S