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.
Dattagupta
Sharmishtha
S
Department of Geosciences, Pennsylvania State University, University Park, PA, USA. sdattag@uni-goettingen.de
Schaperdoth
Irene
I
Montanari
Alessandro
A
Mariani
Sandro
S
Kita
Noriko
N
Valley
John W
JW
Macalady
Jennifer L
JL
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