The sulfidic Frasassi cave system affords a unique opportunity to investigate niche relationships among sulfur-oxidizing bacteria, including epsilonproteobacterial clades with no cultivated representatives. Oxygen and sulfide concentrations in the cave waters range over more than two orders of magnitude as a result of seasonally and spatially variable dilution of the sulfidic groundwater. A full-cycle rRNA approach was used to quantify dominant populations in biofilms collected in both diluted and undiluted zones. Sulfide concentration profiles within biofilms were obtained in situ using microelectrode voltammetry. Populations in rock-attached streamers depended on the sulfide/oxygen supply ratio of bulk water (r ¼ 0.97; Po0.0001). Filamentous epsilonproteobacteria dominated at high sulfide to oxygen ratios (4150), whereas Thiothrix dominated at low ratios (o75). In contrast, Beggiatoa was the dominant group in biofilms at the sediment-water interface regardless of sulfide and oxygen concentrations or supply ratio. Our results highlight the versatility and ecological success of Beggiatoa in diffusion-controlled niches, and demonstrate that high sulfide/oxygen ratios in turbulent water are important for the growth of filamentous epsilonproteobacteria.
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.
BackgroundThe sulfide-rich Frasassi caves in central Italy contain a rare example of a freshwater ecosystem supported entirely by chemoautotrophy. Niphargus ictus, the sole amphipod species previously reported from this locality, was recently shown to host the first known case of a freshwater chemoautotrophic symbiosis. Since the habitat of N. ictus is highly fragmented and is comprised of streams and lakes with various sulfide concentrations, we conducted a detailed study to examine the potential genetic diversity of this species within Frasassi.ResultsBy sequencing one nuclear (ITS) and two mitochondrial (COI and 12S) regions, we show that four partially sympatric Niphargus clades are present in Frasassi. Morphological and behavioral data obtained for three of these clades are perfectly congruent with this molecular delineation and make it possible to distinguish them in the field. Phylogenetic analyses of 28S ribosomal DNA sequences reveal that, among the four clades, only two are closely related to each other. Moreover, these four clades occupy distinct niches that seem to be related to the chemical properties and flow regimes of the various water bodies within Frasassi.ConclusionsOur results suggest that four distinct Niphargus species are present in Frasassi and that they originated from three or four independent invasions of the cave system. At least two among the four species harbor Thiothrix epibionts, which paves the way for further studies of the specificity and evolutionary history of this symbiosis.
-1 (Freytag et al., 2001), levels in the sediment underlying them are typically greater than 1.5·mmol·l -1 (Julian et al., 1999). L. luymesi obtains sulfide from the sediment using long, root-like, posterior extensions of its body (Freytag et al., 2001; Julian et Lamellibrachia luymesi (Polychaeta, Siboglinidae) is a deep-sea vestimentiferan tubeworm that forms large bushlike aggregations at hydrocarbon seeps in the Gulf of Mexico. Like all vestimentiferans, L. luymesi obtains its nutrition from sulfide-oxidizing endosymbiotic bacteria, which it houses in an internal organ called the trophosome. This tubeworm has a lifespan of over 170·years and its survival is contingent upon the availability of sulfide during this long period. In sediments underlying L. luymesi aggregations, microbes produce sulfide by coupling sulfate reduction with hydrocarbon oxidation. L. luymesi acquires sulfide from the sediment using a rootlike posterior extension of its body that is buried in the sediment. Its symbionts then oxidize the sulfide to produce energy for carbon fixation, and release sulfate and hydrogen ions as byproducts. It is critical for the tubeworm to eliminate these waste ions, and it could do so either across its vascular plume or across its root. In this study, we measured sulfate and proton elimination rates from live L. luymesi and found that they eliminated approximately 85% of the sulfate produced by sulfide oxidation, and approximately 67% of the protons produced by various metabolic processes, across their roots. On the basis of experiments using membrane transport inhibitors, we suggest that L. luymesi has anion exchangers that mediate sulfate elimination coupled with bicarbonate uptake. Roots could be the ideal exchange surface for eliminating sulfate and hydrogen ions for two reasons. First, these ions might be eliminated across the root epithelium using facilitated diffusion, which is energetically economical. Second, sulfate and hydrogen ions are substrates for bacterial sulfate reduction, and supplying these ions into the sediment might help ensure a sustained sulfide supply for L. luymesi over its entire lifespan.
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.
hi@scite.ai
10624 S. Eastern Ave., Ste. A-614
Henderson, NV 89052, USA
Copyright © 2024 scite LLC. All rights reserved.
Made with 💙 for researchers
Part of the Research Solutions Family.