Geomicrobiology of a Seawater-Influenced Active Sulfuric Acid Cave

PLoS One. 2019 Aug 8;14(8):e0220706. doi: 10.1371/journal.pone.0220706. eCollection 2019.

Abstract

Fetida Cave is an active sulfuric acid cave influenced by seawater, showing abundant microbial communities that organize themselves under three main different morphologies: water filaments, vermiculations and moonmilk deposits. These biofilms/deposits have different cave distribution, pH, macro- and microelement and mineralogical composition, carbon and nitrogen content. In particular, water filaments and vermiculations had circumneutral and slightly acidic pH, respectively, both had abundant organic carbon and high microbial diversity. They were rich in macro- and microelements, deriving from mineral dissolution, and, in the case of water filaments, from seawater composition. Vermiculations had different color, partly associated with their mineralogy, and unusual minerals probably due to trapping capacities. Moonmilk was composed of gypsum, poor in organic matter, had an extremely low pH (0-1) and low microbial diversity. Based on 16S rRNA gene analysis, the microbial composition of the biofilms/deposits included autotrophic taxa associated with sulfur and nitrogen cycles and biomineralization processes. In particular, water filaments communities were characterized by bacterial taxa involved in sulfur oxidation and reduction in aquatic, aphotic, microaerophilic/anoxic environments (Campylobacterales, Thiotrichales, Arenicellales, Desulfobacterales, Desulforomonadales) and in chemolithotrophy in marine habitats (Oceanospirillales, Chromatiales). Their biodiversity was linked to the morphology of the water filaments and their collection site. Microbial communities within vermiculations were partly related to their color and showed high abundance of unclassified Betaproteobacteria and sulfur-oxidizing Hydrogenophilales (including Sulfuriferula), and Acidiferrobacterales (including Sulfurifustis), sulfur-reducing Desulfurellales, and ammonia-oxidizing Planctomycetes and Nitrospirae. The microbial community associated with gypsum moonmilk showed the strong dominance (>60%) of the archaeal genus Thermoplasma and lower abundance of chemolithotrophic Acidithiobacillus, metal-oxidizing Metallibacterium, Sulfobacillus, and Acidibacillus. This study describes the geomicrobiology of water filaments, vermiculations and gypsum moonmilk from Fetida Cave, providing insights into the microbial taxa that characterize each morphology and contribute to biogeochemical cycles and speleogenesis of this peculiar seawater-influenced sulfuric acid cave.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacteria / isolation & purification
  • Biodiversity
  • Biofilms
  • Caves / microbiology*
  • Chemoautotrophic Growth
  • Microbiota*
  • Oxidation-Reduction
  • Phylogeny
  • Seawater / chemistry*
  • Sulfur / metabolism
  • Sulfuric Acids / metabolism*

Substances

  • Sulfuric Acids
  • Sulfur
  • sulfuric acid

Grant support

IMDA was supported by University of Bologna (UNIBO) and by the award from Lions Club Napoli Megaride district 108 YA. DG and MC's work was supported by the UNIBO. Funding for microbial analyses was provided by Europlanet 2020 15-EPN1-029 and 17-EPN3-021 grants. Europlanet 2020 RI has received funding from the European Union's Horizon 2020 research and innovation programme under grant agreement No 654208. Further funding was provided by the Spanish project MINECO CGL2016-75590-P with ERDF funds. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.