Dominance of Arcobacter in the white filaments from the thermal sulfidic spring of Fetida Cave (Apulia, southern Italy)

Jurado, Valme; D’Angeli, Ilenia Maria; Martin-Pozas, Tamara; Cappelletti, Martina; Ghezzi, Daniele; Gonzalez-Pimentel, Jose Luis; Cuezva, Soledad; Miller, Ana Z.; Fernández-Cortés, Ángel; Waele, Jo De; Sánchez‐Moral, Sergio; Sáiz‐Jiménez, Cesáreo

doi:10.1016/j.scitotenv.2021.149465

Cited by 8 publications

(6 citation statements)

References 73 publications

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“…that dominates Movile Cave's hypoxic Air Bells microbial mat [ 22 ]. Moreover, Arcobacteraceae family was found dominant in the white filaments from the thermal sulfidic spring of Fetida Cave, Italy [ 56 ]. Sulfur oxidation was not, however, limited to the lakeside sediments.…”

Section: Discussionmentioning

confidence: 99%

Competition-cooperation in the chemoautotrophic ecosystem of Movile Cave: first metagenomic approach on sediments

Chiciudean

Russo

Bogdan

et al. 2022

Environmental Microbiome

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Background Movile Cave (SE Romania) is a chemoautotrophically-based ecosystem fed by hydrogen sulfide-rich groundwater serving as a primary energy source analogous to the deep-sea hydrothermal ecosystems. Our current understanding of Movile Cave microbiology has been confined to the sulfidic water and its proximity, as most studies focused on the water-floating microbial mat and planktonic accumulations likely acting as the primary production powerhouse of this unique subterranean ecosystem. By employing comprehensive genomic-resolved metagenomics, we questioned the spatial variation, chemoautotrophic abilities, ecological interactions and trophic roles of Movile Cave’s microbiome thriving beyond the sulfidic-rich water. Results A customized bioinformatics pipeline led to the recovery of 106 high-quality metagenome-assembled genomes from 7 cave sediment metagenomes. Assemblies’ taxonomy spanned 19 bacterial and three archaeal phyla with Acidobacteriota, Chloroflexota, Proteobacteria, Planctomycetota, Ca. Patescibacteria, Thermoproteota, Methylomirabilota, and Ca. Zixibacteria as prevalent phyla. Functional gene analyses predicted the presence of CO2 fixation, methanotrophy, sulfur and ammonia oxidation in the explored sediments. Species Metabolic Coupling Analysis of metagenome-scale metabolic models revealed the highest competition-cooperation interactions in the sediments collected away from the water. Simulated metabolic interactions indicated autotrophs and methanotrophs as major donors of metabolites in the sediment communities. Cross-feeding dependencies were assumed only towards 'currency' molecules and inorganic compounds (O2, PO43−, H+, Fe2+, Cu2+) in the water proximity sediment, whereas hydrogen sulfide and methanol were assumedly traded exclusively among distant gallery communities. Conclusions These findings suggest that the primary production potential of Movile Cave expands way beyond its hydrothermal waters, enhancing our understanding of the functioning and ecological interactions within chemolithoautotrophically-based subterranean ecosystems.

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Section: Discussionmentioning

confidence: 99%

Competition-cooperation in the chemoautotrophic ecosystem of Movile Cave: first metagenomic approach on sediments

Chiciudean

Russo

Bogdan

et al. 2022

Environmental Microbiome

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“…isolated from Movile Cave’s hypoxic Air Bells microbial mat [22]. Moreover, Arcobacteraceae family was found dominant in the white filaments from the thermal sulfidic spring of Fetida Cave, Italy [56]. Sulfur oxidation was not however limited to the lakeside sediments.…”

Section: Discussionmentioning

confidence: 99%

Competition-cooperation in the chemoautotrophic ecosystem of Movile Cave – first metagenomic approach on sediments

Chiciudean

Russo

Bogdan

et al. 2022

Preprint

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BackgroundMovile Cave (Dobrogea, SE Romania) hosts a subterranean chemoautotrophically-based ecosystem supported by a sulfidic thermal aquifer analogous to the deep-sea hydrothermal ecosystems. Our current understanding of Movile Cave microbiology has been confined to the thermal water proximity (no more than 2 m distant), with most studies focusing on the water-floating mat, which likely acts as the primary production powerhouse in this sulfidic ecosystem. To gain more insightful information on the functioning of the sulfidic Movile Cave ecosystem, we employed a metagenomics-resolved approach to reveal the microbiome diversity, metabolic potential, and interactions and infer its roles within the food webs in the sediments beyond the sulfidic thermal waters.ResultsA customized bioinformatics pipeline led to the recovery of 106 high-quality metagenome-assembled genomes from 7 cave sediment metagenomes. Assemblies’ taxonomy spanned 19 bacterial and three archaeal phyla with Acidobacteriota, Chloroflexota, Proteobacteria, Planctomycetota, Ca. Patescibacteria, Thermoproteota, Methylomirabilota, and Ca. Zixibacteria as prevalent phyla. Functional gene analyses allowed prediction of CO2 fixation, methanotrophy, sulfur and ammonia oxidation as possibly occurring in the explored sediments. Species Metabolic Coupling Analysis of metagenome-scale metabolic models revealed the highest competition-cooperation interactions in the sediments collected at the farthest distance from the sulfidic water. As a result of simulated metabolic interactions, autotrophs and methanotrophs were hypothesized as major donors of exchanged metabolites in the sediment communities. Cross-feeding dependencies were assumed only towards ‘currency’ molecules and inorganic compounds (O2, PO43-, H+, Fe2+, Cu2+) in the sediment nearby sulfidic water, whereas hydrogen sulfide and methanol are predictably traded exclusively among communities dwelling in the distant gallery.ConclusionsThese findings suggest that the primary production potential of the Movile Cave expands way beyond its hydrothermal waters, enhancing our understanding of ecological interactions inside chemolithoautotrophically based subterranean ecosystems and their functioning.

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“…The phyla pattern of microbial mats on the rock surface of volcanic caves (lava tubes) was obtained from Gonzalez-Pimentel et al (2018) , Gonzalez-Pimentel et al (2021) , Nicolosi et al (2023) . The phyla pattern of biofilms thriving as streamers and sedimented filaments in the water of SAS caves was obtained from D’Angeli et al (2019a) , Jurado et al (2021) . The boundaries for the first and third quartiles are shown (box length), with the centerline representing the median, the symbol (†) indicating the average, and the whiskers representing the maximum/minimum values.…”

Section: Microbial Diversity In Cavesmentioning

confidence: 99%

“…Beggiatoa ( Thiotrichales, Gammaproteobacteria ) was the dominant group in locations where the shear stress caused by the flowing water is low enough to allow fine sediment accumulation, regardless of sulfide and oxygen concentration ( Macalady et al, 2008 ). In the sulfidic spring of Fetida Cave, Italy, the microbial biomass of water filaments was dominated by the genus Arcobacter within the phylum Campylobacterota ( Jurado et al, 2021 ). Notably, Arcobacte r species are primary producers because capable of fixing CO 2 and growing chemolithotrophically via sulfur oxidation.…”

Section: Microbial Diversity In Cavesmentioning

confidence: 99%

The geomicrobiology of limestone, sulfuric acid speleogenetic, and volcanic caves: basic concepts and future perspectives

Turrini,

Chebbi,

Riggio

et al. 2024

Front. Microbiol.

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Caves are ubiquitous subterranean voids, accounting for a still largely unexplored surface of the Earth underground. Due to the absence of sunlight and physical segregation, caves are naturally colonized by microorganisms that have developed distinctive capabilities to thrive under extreme conditions of darkness and oligotrophy. Here, the microbiomes colonizing three frequently studied cave types, i.e., limestone, sulfuric acid speleogenetic (SAS), and lava tubes among volcanic caves, have comparatively been reviewed. Geological configurations, nutrient availability, and energy flows in caves are key ecological drivers shaping cave microbiomes through photic, twilight, transient, and deep cave zones. Chemoheterotrophic microbial communities, whose sustenance depends on nutrients supplied from outside, are prevalent in limestone and volcanic caves, while elevated inorganic chemical energy is available in SAS caves, enabling primary production through chemolithoautotrophy. The 16S rRNA-based metataxonomic profiles of cave microbiomes were retrieved from previous studies employing the Illumina platform for sequencing the prokaryotic V3-V4 hypervariable region to compare the microbial community structures from different cave systems and environmental samples. Limestone caves and lava tubes are colonized by largely overlapping bacterial phyla, with the prevalence of Pseudomonadota and Actinomycetota, whereas the co-dominance of Pseudomonadota and Campylobacterota members characterizes SAS caves. Most of the metataxonomic profiling data have so far been collected from the twilight and transient zones, while deep cave zones remain elusive, deserving further exploration. Integrative approaches for future geomicrobiology studies are suggested to gain comprehensive insights into the different cave types and zones. This review also poses novel research questions for unveiling the metabolic and genomic capabilities of cave microorganisms, paving the way for their potential biotechnological applications.

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Dominance of Arcobacter in the white filaments from the thermal sulfidic spring of Fetida Cave (Apulia, southern Italy)

Cited by 8 publications

References 73 publications

Competition-cooperation in the chemoautotrophic ecosystem of Movile Cave: first metagenomic approach on sediments

Competition-cooperation in the chemoautotrophic ecosystem of Movile Cave: first metagenomic approach on sediments

Competition-cooperation in the chemoautotrophic ecosystem of Movile Cave – first metagenomic approach on sediments

The geomicrobiology of limestone, sulfuric acid speleogenetic, and volcanic caves: basic concepts and future perspectives

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