Geomicrobiology of a seawater-influenced active sulfuric acid cave

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...

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Published inPloS one Vol. 14; no. 8; p. e0220706
Main Authors D'Angeli, Ilenia M, Ghezzi, Daniele, Leuko, Stefan, Firrincieli, Andrea, Parise, Mario, Fiorucci, Adriano, Vigna, Bartolomeo, Addesso, Rosangela, Baldantoni, Daniela, Carbone, Cristina, Miller, Ana Zelia, Jurado, Valme, Saiz-Jimenez, Cesareo, De Waele, Jo, Cappelletti, Martina
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 08.08.2019
Public Library of Science (PLoS)
Subjects
Abundance
Acidification
Ammonia
Aquatic environment
Aquatic habitats
Bacteria - isolation & purification
Biodiversity
Biofilms
Biogeochemical cycles
Biology
Biology and Life Sciences
Carbon
Caves
Caves - microbiology
Chemical analysis
Chemical properties
Chemoautotrophic Growth
Chemoautotrophy
Color
Communities
Composition
Deposits
Earth Sciences
Ecology and Environmental Sciences
Ecosystem biology
Ecosystems
Environmental aspects
Environmental science
Filaments
Genes
Genetic research
Genomes
Geology
Gypsum
Identification and classification
Influence
Metabolism
Microbial activity
Microbial colonies
Microbiota
Microorganisms
Mineralization
Mineralogy
Minerals
Morphology
Nitrogen
Nitrogen content
Organic carbon
Organic matter
Oxidation
Oxidation-Reduction
Oxidation-reduction reactions
pH effects
Pharmacy
Phylogeny
Physical Sciences
RNA
rRNA 16S
Seawater
Seawater - chemistry
Seawater composition
Sulfur
Sulfur - metabolism
Sulfur compounds
Sulfur oxidation
Sulfuric acid
Sulfuric Acids - metabolism
Taxa
Trace elements
Water
Water analysis
Italy
Spain
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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.
AbstractList 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.
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.
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.
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.
Audience Academic
Author Vigna, Bartolomeo
Miller, Ana Zelia
Addesso, Rosangela
D'Angeli, Ilenia M
Ghezzi, Daniele
Leuko, Stefan
Jurado, Valme
Parise, Mario
Baldantoni, Daniela
Saiz-Jimenez, Cesareo
Fiorucci, Adriano
Firrincieli, Andrea
Carbone, Cristina
De Waele, Jo
Cappelletti, Martina
AuthorAffiliation 8 DISTAV, Department of Geological, Environmental and Biological Sciences, University of Genoa, Genoa, Italy
1 Department of Biological, Geological and Environmental Sciences, University of Bologna, Bologna, Italy
6 Department of Environment, Land and Infrastructure Engineering, Polytechnic University of Turin, Torino, Italy
The University of Akron, UNITED STATES
7 Department of Chemistry and Biology “Adolfo Zambelli”, University of Salerno, Fisciano (SA), Italy
3 DLR Institute of Aerospace Medicine, Radiation Biology, Köln, Germany
9 HERCULES Laboratory, University of Évora, Évora, Portugal
4 School of Environmental and Forest Science, University of Washington, Seattle, WA, United States of America
2 Department of Pharmacy and Biotechnology, University of Bologna, Bologna, Italy
5 Department of Geological and Environmental Sciences, University of Bari “Aldo Moro”, Bari, Italy
10 Instituto de Recursos Naturales y Agrobiologia, IRNAS-CSIC, Sevilla, Spain
AuthorAffiliation_xml – name: 8 DISTAV, Department of Geological, Environmental and Biological Sciences, University of Genoa, Genoa, Italy
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– name: 4 School of Environmental and Forest Science, University of Washington, Seattle, WA, United States of America
– name: 10 Instituto de Recursos Naturales y Agrobiologia, IRNAS-CSIC, Sevilla, Spain
– name: 3 DLR Institute of Aerospace Medicine, Radiation Biology, Köln, Germany
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  organization: Department of Geological and Environmental Sciences, University of Bari "Aldo Moro", Bari, Italy
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/31393920$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright COPYRIGHT 2019 Public Library of Science
2019 D’Angeli et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
2019 D’Angeli et al 2019 D’Angeli et al
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– notice: 2019 D’Angeli et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
– notice: 2019 D’Angeli et al 2019 D’Angeli et al
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Snippet Fetida Cave is an active sulfuric acid cave influenced by seawater, showing abundant microbial communities that organize themselves under three main different...
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SubjectTerms Abundance
Acidification
Ammonia
Aquatic environment
Aquatic habitats
Bacteria - isolation & purification
Biodiversity
Biofilms
Biogeochemical cycles
Biology
Biology and Life Sciences
Carbon
Caves
Caves - microbiology
Chemical analysis
Chemical properties
Chemoautotrophic Growth
Chemoautotrophy
Color
Communities
Composition
Deposits
Earth Sciences
Ecology and Environmental Sciences
Ecosystem biology
Ecosystems
Environmental aspects
Environmental science
Filaments
Genes
Genetic research
Genomes
Geology
Gypsum
Identification and classification
Influence
Metabolism
Microbial activity
Microbial colonies
Microbiota
Microorganisms
Mineralization
Mineralogy
Minerals
Morphology
Nitrogen
Nitrogen content
Organic carbon
Organic matter
Oxidation
Oxidation-Reduction
Oxidation-reduction reactions
pH effects
Pharmacy
Phylogeny
Physical Sciences
RNA
rRNA 16S
Seawater
Seawater - chemistry
Seawater composition
Sulfur
Sulfur - metabolism
Sulfur compounds
Sulfur oxidation
Sulfuric acid
Sulfuric Acids - metabolism
Taxa
Trace elements
Water
Water analysis
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Title Geomicrobiology of a seawater-influenced active sulfuric acid cave
URI https://www.ncbi.nlm.nih.gov/pubmed/31393920
https://www.proquest.com/docview/2270187867/abstract/
https://search.proquest.com/docview/2270008603
https://pubmed.ncbi.nlm.nih.gov/PMC6687129
https://doaj.org/article/81d2166c6bec4d6986025b2f02c6b298
http://dx.doi.org/10.1371/journal.pone.0220706
Volume 14
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