Dataset Information

Capturing the microbial dark matter in desert soils using culturomics-based metagenomics and high-resolution analysis.

ABSTRACT: Deserts occupy one-third of the Earth's terrestrial surface and represent a potentially significant reservoir of microbial biodiversity, yet the majority of desert microorganisms remain uncharacterized and are seen as "microbial dark matter". Here, we introduce a multi-omics strategy, culturomics-based metagenomics (CBM) that integrates large-scale cultivation, full-length 16S rRNA gene amplicon, and shotgun metagenomic sequencing. The results showed that CBM captured a significant amount of taxonomic and functional diversity missed in direct sequencing by increasing the recovery of amplicon sequence variants (ASVs) and high/medium-quality metagenome-assembled genomes (MAGs). Importantly, CBM allowed the post hoc recovery of microbes of interest (e.g., novel or specific taxa), even those with extremely low abundance in the culture. Furthermore, strain-level analyses based on CBM and direct sequencing revealed that the desert soils harbored a considerable number of novel bacterial candidates (1941, 51.4%), of which 1095 (from CBM) were culturable. However, CBM would not exactly reflect the relative abundance of true microbial composition and functional pathways in the in situ environment, and its use coupled with direct metagenomic sequencing could provide greater insight into desert microbiomes. Overall, this study exemplifies the CBM strategy with high-resolution is an ideal way to deeply explore the untapped novel bacterial resources in desert soils, and substantially expands our knowledge on the microbial dark matter hidden in the vast expanse of deserts.

SUBMITTER: Li S

PROVIDER: S-EPMC10516943 | biostudies-literature | 2023 Sep

REPOSITORIES: biostudies-literature

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Publications

Capturing the microbial dark matter in desert soils using culturomics-based metagenomics and high-resolution analysis.

Li Shuai S Lian Wen-Hui WH Han Jia-Rui JR Ali Mukhtiar M Lin Zhi-Liang ZL Liu Yong-Hong YH Li Li L Zhang Dong-Ya DY Jiang Xian-Zhi XZ Li Wen-Jun WJ Dong Lei L

NPJ biofilms and microbiomes 20230922 1

Deserts occupy one-third of the Earth's terrestrial surface and represent a potentially significant reservoir of microbial biodiversity, yet the majority of desert microorganisms remain uncharacterized and are seen as "microbial dark matter". Here, we introduce a multi-omics strategy, culturomics-based metagenomics (CBM) that integrates large-scale cultivation, full-length 16S rRNA gene amplicon, and shotgun metagenomic sequencing. The results showed that CBM captured a significant amount of tax ...[more]

PMID: 37736746

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Project description:BackgroundThe microbiome of the Sinai Desert farming system plays an important role in the adaptive strategy of growing crops in a harsh, poly-extreme, desert environment. However, the diversity and function of microbial communities under this unfavorable moisture and nutritional conditions have not yet been investigated. Based on culturomic and metagenomic methods, we analyzed the microbial diversity and function of a total of fourteen rhizosphere soil samples (collected from twelve plants in four farms of the Sinai desert), which may provide a valuable and meaningful guidance for the design of microbial inoculants.ResultsThe results revealed a wide range of microbial taxa, including a high proportion of novel undescribed lineages. The composition of the rhizosphere microbial communities differed according to the sampling sites, despite similarities or differences in floristics. Whereas, the functional features of rhizosphere microbiomes were significantly similar in different sampling sites, although the microbial communities and the plant hosts themselves were different. Importantly, microorganisms involved in ecosystem functions are different between the sampling sites, for example nitrogen fixation was prevalent in all sample sites while microorganisms responsible for this process were different.ConclusionHere, we provide the first characterization of microbial communities and functions of rhizosphere soil from the Sinai desert farming systems and highlight its unexpectedly high diversity. This study provides evidence that the key microorganisms involved in ecosystem functions are different between sampling sites with different environment conditions, emphasizing the importance of the functional microbiomes of rhizosphere microbial communities. Furthermore, we suggest that microbial inoculants to be used in future agricultural production should select microorganisms that can be involved in plant-microorganism interactions and are already adapted to a similar environmental setting.

Project description:Although microorganisms constitute the most diverse and abundant life form on Earth, in many environments, the vast majority of them remain uncultured. As it is based on information gleaned mainly from cultivated microorganisms, our current body of knowledge regarding microbial life is partial and does not reflect actual microbial diversity. That diversity is hidden in the uncultured microbial majority, termed by microbiologists as "microbial dark matter" (MDM), a term borrowed from astrophysics. Metagenomic sequencing analysis techniques (both 16S rRNA gene and shotgun sequencing) compare gene sequences to reference databases, each of which represents only a small fraction of the existing microorganisms. Unaligned sequences lead to groups of "unknown microorganisms" that are usually ignored and rarefied from diversity analysis. To address this knowledge gap, we analyzed the 16S rRNA gene sequences of microbial communities from four different environments-a living organism, a desert environment, a natural aquatic environment, and a membrane bioreactor for wastewater treatment. From those datasets, we chose representative sequences of potentially unknown bacteria for additional examination as "microbial dark matter sequences" (MDMS). Sequence existence was validated by specific amplification and re-sequencing. These sequences were screened against databases and aligned to the Genome Taxonomy Database to build a comprehensive phylogenetic tree for additional sequence classification, revealing potentially new candidate phyla and other lineages. These putative MDMS were also screened against metagenome-assembled genomes from the explored environments for additional validation and for taxonomic and metabolic characterizations. This study shows the immense importance of MDMS in environmental metataxonomic analyses of 16S rRNA gene sequences and provides a simple and readily available methodology for the examination of MDM hidden behind amplicon sequencing results.

Dataset Information

Capturing the microbial dark matter in desert soils using culturomics-based metagenomics and high-resolution analysis.

Publications

Capturing the microbial dark matter in desert soils using culturomics-based metagenomics and high-resolution analysis.

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