Insights into the microbial life in silica-rich subterranean environments: microbial communities and ecological interactions in an orthoquartzite cave (Imawarì Yeuta, Auyan Tepui, Venezuela).

Daniele Ghezzi, Lisa Foschi, Andrea Firrincieli, Pei-Ying Hong, Freddy Vergara, Jo De Waele, Francesco Sauro, Martina Cappelletti

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1 Scopus citations

Abstract

Microbial communities inhabiting caves in quartz-rich rocks are still underexplored, despite their possible role in the silica cycle. The world’s longest orthoquartzite cave, Imawarì Yeuta, represents a perfect arena for the investigation of the interactions between microorganisms and silica in non-thermal environments due to the presence of extraordinary amounts of amorphous silica speleothems of different kinds. In this work, the microbial diversity of Imawarì Yeuta was dissected by analyzing nineteen samples collected from different locations representative of different silica amorphization phases and types of samples. Specifically, we investigated the major ecological patterns in cave biodiversity, specific taxa enrichment, and the main ecological clusters through co-occurrence network analysis. Water content greatly contributed to the microbial communities’ composition and structures in the cave leading to the sample clustering into three groups DRY, WET, and WATER. Each of these groups was enriched in members of Actinobacteriota, Acidobacteriota, and Gammaproteobacteria, respectively. Alpha diversity analysis showed the highest value of diversity and richness for the WET samples, while the DRY group had the lowest. This was accompanied by the presence of correlation patterns including either orders belonging to various phyla from WET samples or orders belonging to the Actinobacteriota and Firmicutes phyla from DRY group samples. The phylogenetic analysis of the dominant species in WET and DRY samples showed that Acidobacteriota and Actinobacteriota strains were affiliated with uncultured bacteria retrieved from various oligotrophic and silica/quartz-rich environments, not only associated with subterranean sites. Our results suggest that the water content greatly contributes to shaping the microbial diversity within a subterranean quartzite environment. Further, the phylogenetic affiliation between Imawarì Yeuta dominant microbes and reference strains retrieved from both surface and subsurface silica- and/or CO2/CO-rich environments, underlines the selective pressure applied by quartz as rock substrate. Oligotrophy probably in association with the geochemistry of silica/quartz low pH buffering activity and alternative energy sources led to the colonization of specific silica-associated microorganisms. This study provides clues for a better comprehension of the poorly known microbial life in subsurface and surface quartz-dominated environments.
Original languageEnglish (US)
JournalFrontiers in microbiology
Volume13
DOIs
StatePublished - Sep 23 2022

Bibliographical note

KAUST Repository Item: Exported on 2022-10-13
Acknowledgements: We thank Leonardo Piccini for his contribution in the sample collection, Hosam Zowawi for supporting contacts with KAUST and for further advancement of the research project in the last years, and Laura Negretti for technical assistance in SEM and FESEM analyses. We also thank Cristina Carbone (Dip. DISTAV, University of Genova) for her help with the investigations on mineral phases and EDS, and Andrea Columbu for the XRF analyses. Our gratitude goes to Christine Moissl-Eichinger, Kaisa Koskinen Mora, Alexander Mahnert, Slave Trajanoski, and Lisa Wink at the Medical University of Graz (Austria) for their help with sample preparation for Illumina sequencing and data analysis of EMIRGE data. We acknowledge the agencies and associations involved in granting the permit for the speleological expeditions and sample collection: Instituto National de Parques and the patronage of the Government of Bolivar State from Venezuela, the Embassy of the Bolivarian Republic of Venezuela in Italy. This article has been developed in the framework of the Rolex Award of Enterprise supporting Francesco Sauro in research and exploration on the tepui highlands of South America. We are grateful to UNIBO student Andrea Gozzi for his support with the experimental work. We acknowledge the Rector Francesco Ubertini, the Vice-Rector for Research A. Rotolo, and the Governing Academic Bodies of the University of Bologna (UNIBO) for the financial support of the research project and the PhD scholarship for DG. The research activities were also partly supported by RFO UNIBO grants. Funding for EMIRGE analysis was provided by Europlanet 2020 17-EPN3-026 grant. Europlanet 2020 RI has received funding from the European Union’s Horizon 2020 research and innovation program under grant agreement No 654208.

ASJC Scopus subject areas

  • Microbiology (medical)
  • Microbiology

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