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Bacteria and Metabolic Potential in Karst Caves Revealed by Intensive Bacterial Cultivation and Genome Assembly.

ABSTRACT: Karst caves are widely distributed subsurface systems, and the microbiomes therein are proposed to be the driving force for cave evolution and biogeochemical cycling. In past years, culture-independent studies on the microbiomes of cave systems have been conducted, yet intensive microbial cultivation is still needed to validate the sequence-derived hypothesis and to disclose the microbial functions in cave ecosystems. In this study, the microbiomes of two karst caves in Guizhou Province in southwest China were examined. A total of 3,562 bacterial strains were cultivated from rock, water, and sediment samples, and 329 species (including 14 newly described species) of 102 genera were found. We created a cave bacterial genome collection of 218 bacterial genomes from a karst cave microbiome through the extraction of 204 database-derived genomes and de novo sequencing of 14 new bacterial genomes. The cultivated genome collection obtained in this study and the metagenome data from previous studies were used to investigate the bacterial metabolism and potential involvement in the carbon, nitrogen, and sulfur biogeochemical cycles in the cave ecosystem. New N₂-fixing Azospirillum and alkane-oxidizing Oleomonas species were documented in the karst cave microbiome. Two pcaIJ clusters of the β-ketoadipate pathway that were abundant in both the cultivated microbiomes and the metagenomic data were identified, and their representatives from the cultivated bacterial genomes were functionally demonstrated. This large-scale cultivation of a cave microbiome represents the most intensive collection of cave bacterial resources to date and provides valuable information and diverse microbial resources for future cave biogeochemical research.IMPORTANCE Karst caves are oligotrophic environments that are dark and humid and have a relatively stable annual temperature. The diversity of bacteria and their metabolisms are crucial for understanding the biogeochemical cycling in cave ecosystems. We integrated large-scale bacterial cultivation with metagenomic data mining to explore the compositions and metabolisms of the microbiomes in two karst cave systems. Our results reveal the presence of a highly diversified cave bacterial community, and 14 new bacterial species were described and their genomes sequenced. In this study, we obtained the most intensive collection of cultivated microbial resources from karst caves to date and predicted the various important routes for the biogeochemical cycling of elements in cave ecosystems.

SUBMITTER: Zhu HZ

PROVIDER: S-EPMC8105019 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Nitrite-oxidizing bacteria (NOB) are ubiquitous and abundant microorganisms that play key roles in global nitrogen and carbon biogeochemical cycling. Despite recent advances in understanding NOB physiology and taxonomy, currently very few cultured NOB or representative NOB genome sequences from marine environments exist. In this study, we employed enrichment culturing and genomic approaches to shed light on the phylogeny and metabolic capacity of marine NOB. We successfully enriched two marine NOB (designated MSP and DJ) and obtained a high-quality metagenome-assembled genome (MAG) from each organism. The maximum nitrite oxidation rates of the MSP and DJ enrichment cultures were 13.8 and 30.0 μM nitrite per day, respectively, with these optimum rates occurring at 0.1 mM and 0.3 mM nitrite, respectively. Each enrichment culture exhibited a different tolerance to various nitrite and salt concentrations. Based on phylogenomic position and overall genome relatedness indices, both NOB MAGs were proposed as novel taxa within the Nitrospinota and Nitrospirota phyla. Functional predictions indicated that both NOB MAGs shared many highly conserved metabolic features with other NOB. Both NOB MAGs encoded proteins for hydrogen and organic compound metabolism and defense mechanisms for oxidative stress. Additionally, these organisms may have the genetic potential to produce cobalamin (an essential enzyme cofactor that is limiting in many environments) and, thus, may play an important role in recycling cobalamin in marine sediment. Overall, this study appreciably expands our understanding of the Nitrospinota and Nitrospirota phyla and suggests that these NOB play important biogeochemical roles in marine habitats.IMPORTANCE Nitrification is a key process in the biogeochemical and global nitrogen cycle. Nitrite-oxidizing bacteria (NOB) perform the second step of aerobic nitrification (converting nitrite to nitrate), which is critical for transferring nitrogen to other organisms for assimilation or energy. Despite their ecological importance, there are few cultured or genomic representatives from marine systems. Here, we obtained two NOB (designated MSP and DJ) enriched from marine sediments and estimated the physiological and genomic traits of these marine microbes. Both NOB enrichment cultures exhibit distinct responses to various nitrite and salt concentrations. Genomic analyses suggest that these NOB are metabolically flexible (similar to other previously described NOB) yet also have individual genomic differences that likely support distinct niche distribution. In conclusion, this study provides more insights into the ecological roles of NOB in marine environments.

Project description:The geological role of microorganisms has been widely studied in the karst cave ecosystem. However, microbial interactions and ecological functions in such a dark, humid, and oligotrophic habitat have received far less attention, which is crucial to understanding cave biogeochemistry. Herein, microorganisms from weathered rock and sediment along the Heshang Cave depth were analyzed by random matrix theory-based network and Tax4Fun functional prediction. The results showed that although the cave microbial communities have spatial heterogeneity, differential habitats drove the community structure and diversity. Actinobacteria were predominant in weathered rock, whereas Proteobacteria dominated the sediment. The sediment communities presented significantly higher alpha diversities due to the relatively abundant nutrition from the outside by the intermittent stream. Consistently, microbial interactions in sediment were more complex, as visualized by more nodes and links. The abundant taxa presented more positive correlations with other community members in both of the two networks, indicating that they relied on promotion effects to adapt to the extreme environment. The keystones in weathered rock were mainly involved in the biodegradation of organic compounds, whereas the keystone Nitrospira in sediment contributed to carbon/nitrogen fixation. Collectively, these findings suggest that microbial interactions may lead to distinct taxonomic and functional communities in weathered rock and sediment in the subsurface Heshang Cave. IMPORTANCE In general, the constant physicochemical conditions and limited nutrient sources over long periods in the subsurface support a stable ecosystem in karst cave. Previous studies on cave microbial ecology were mostly focused on community composition, diversity, and the relationship with local environmental factors. There are still many unknowns about the microbial interactions and functions in such a dark environment with little human interference. Two representative habitats, including weathered rock and sediment in Heshang Cave, were selected to give an integrated insight into microbial interactions and potential functions. The cooccurrence network, especially the subnetwork, was used to characterize the cave microbial interactions in detail. We demonstrated that abundant taxa primarily relied on promotion effects rather than inhibition effects to survive in Heshang Cave. Keystone species may play important metabolic roles in sustaining ecological functions. Our study provides improved understanding of microbial interaction patterns and community ecological functions in the karst cave ecosystem.

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Bacteria and Metabolic Potential in Karst Caves Revealed by Intensive Bacterial Cultivation and Genome Assembly.

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