Geomicrobiology of a seawater-influenced active sulfuric acid cave

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.

Microbial Communities in Vermiculation Deposits from an Alpine Cave

“…Conversely, it was clear that the comparison of the microbial communities from Morgana Cave vermiculations with those of the Frasassi and Fetida sulfuric acid caves revealed striking differences, due to the extremely different environments (alkaline in Morgana and highly acid in sulfuric caves). In fact, Fetida Cave vermiculations showed high abundance of unclassified Betaproteobacteria and sulfur-oxidizing Hydrogenophilales (including Sulfuriferula), Acidiferrobacterales (including Sulfurifustis), sulfur-reducing Desulfurellales, and ammoniaoxidizing Planctomycetes and Nitrospirae (D'Angeli et al, 2019b).…”

“…Vermiculation deposits are among the most characteristic features of Morgana Cave. Vermiculation patterns developing on wall surfaces have been found in many caves around the world (Hose and Macalady, 2006;Merino et al, 2014;Bojar et al, 2015;Faucher and Lauriol, 2016;D'Angeli et al, 2017D'Angeli et al, , 2019aD'Angeli et al, , 2019bAddesso et al, 2020).…”

Transition from unclassified Ktedonobacterales to Actinobacteria during amorphous silica precipitation in a quartzite cave environment

“…The reads were first trimmed for the indexes and primer sequences, and then checked for chimera and quality by using QIIME2 software. Reads were analysed using the DADA2 package version 1.5.0, as previously described in D’Angeli et al 79 . Universal primer pairs 9F-1406R and 344F-1406R were respectively used to amplify the near full-length bacterial and archaeal 16S rRNA genes following PCR amplification procedures described by Koskinen et al 80 .…”

Insights into the Geomicrobiology of Biovermiculations from Rock Billet Incubation Experiments

“…Biovermiculation microbial communities have been studied using rRNA gene sequencing from multiple limestone caves, and typically contain diverse microbial communities dominated by Proteobacteria , Actinobacteria , Acidobacteria , and several other phyla [ 5 , 9 , 55 , 56 , 57 ]. However, less is known about biovermiculations from lava caves.…”

“…We use the term “biovermiculation” here in sensu Hose et al [ 8 ], who found substantial microbial biomass and biofilm in biovermiculations from sulfide-rich Villa Luz cave. This term is now used more broadly, based on the recognition of a substantial microbial content in vermiculations in many cave systems (e.g., [ 6 , 7 , 9 ]). Similar formations have also been observed at the sub-millimeter scale in cyanobacterial hypoliths on the underside of a translucent rock in Strzelecki Desert, Australia [ 10 ] as well as in higher vegetation patterns in the Negev Desert, Israel that exhibit biovermiculation geometry on a multi-meter scale [ 11 ].…”