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Function-based rhizosphere assembly along a gradient of desiccation in the former Aral Sea

  • The desiccation of the Aral Sea represents one of the largest human-made environmental regional disasters. The salt- and toxin-enriched dried-out basin provides a natural laboratory for studying ecosystem functioning and rhizosphere assembly under extreme anthropogenic conditions. Here, we investigated the prokaryotic rhizosphere communities of the native pioneer plant Suaeda acuminata (C.A.Mey.) Moq. in comparison to bulk soil across a gradient of desiccation (5, 10, and 40 years) by metagenome and amplicon sequencing combined with quantitative PCR (qPCR) analyses. The rhizosphere effect was evident due to significantly higher bacterial abundances but less diversity in the rhizosphere compared to bulk soil. Interestingly, in the highest salinity (5 years of desiccation), rhizosphere functions were mainly provided by archaeal communities. Along the desiccation gradient, we observed a significant change in the rhizosphere microbiota, which was reflected by (i) a decreasing archaeon-bacterium ratio, (ii) replacement of halophilicThe desiccation of the Aral Sea represents one of the largest human-made environmental regional disasters. The salt- and toxin-enriched dried-out basin provides a natural laboratory for studying ecosystem functioning and rhizosphere assembly under extreme anthropogenic conditions. Here, we investigated the prokaryotic rhizosphere communities of the native pioneer plant Suaeda acuminata (C.A.Mey.) Moq. in comparison to bulk soil across a gradient of desiccation (5, 10, and 40 years) by metagenome and amplicon sequencing combined with quantitative PCR (qPCR) analyses. The rhizosphere effect was evident due to significantly higher bacterial abundances but less diversity in the rhizosphere compared to bulk soil. Interestingly, in the highest salinity (5 years of desiccation), rhizosphere functions were mainly provided by archaeal communities. Along the desiccation gradient, we observed a significant change in the rhizosphere microbiota, which was reflected by (i) a decreasing archaeon-bacterium ratio, (ii) replacement of halophilic archaea by specific plant-associated bacteria, i.e., Alphaproteobacteria and Actinobacteria, and (iii) an adaptation of specific, potentially plant-beneficial biosynthetic pathways. In general, both bacteria and archaea were found to be involved in carbon cycling and fixation, as well as methane and nitrogen metabolism. Analysis of metagenome-assembled genomes (MAGs) showed specific signatures for production of osmoprotectants, assimilatory nitrate reduction, and transport system induction. Our results provide evidence that rhizosphere assembly by cofiltering specific taxa with distinct traits is a mechanism which allows plants to thrive under extreme conditions. Overall, our findings highlight a function-based rhizosphere assembly, the importance of plant-microbe interactions in salinated soils, and their exploitation potential for ecosystem restoration approaches.IMPORTANCE The desertification of the Aral Sea basin in Uzbekistan and Kazakhstan represents one of the most serious anthropogenic environmental disasters of the last century. Since the 1960s, the world's fourth-largest inland body of water has been constantly shrinking, which has resulted in an extreme increase of salinity accompanied by accumulation of many hazardous and carcinogenic substances, as well as heavy metals, in the dried-out basin. Here, we investigated bacterial and archaeal communities in the rhizosphere of pioneer plants by combining classic molecular methods with amplicon sequencing as well as metagenomics for functional insights. By implementing a desiccation gradient, we observed (i) remarkable differences in the archaeon-bacterium ratio of plant rhizosphere samples, (ii) replacement of archaeal indicator taxa during succession, and (iii) the presence of specific, potentially plant-beneficial biosynthetic pathways in archaea present during the early stages. In addition, our results provide hitherto-undescribed insights into the functional redundancy between plant-associated archaea and bacteria. The desertification of the Aral Sea basin in Uzbekistan and Kazakhstan represents one of the most serious anthropogenic environmental disasters of the last century. Since the 1960s, the world's fourth-largest inland body of water has been constantly shrinking, which has resulted in an extreme increase of salinity accompanied by accumulation of many hazardous and carcinogenic substances, as well as heavy metals, in the dried-out basin.show moreshow less

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Author details:Wisnu Adi WicaksonoORCiD, Dilfuza Egamberdieva, Christian Berg, Maximilian Mora, Peter KusstatscherORCiD, Tomislav CernavaORCiDGND, Gabriele BergORCiDGND
DOI:https://doi.org/10.1128/msystems.00739-22
ISSN:2379-5077
Pubmed ID:https://pubmed.ncbi.nlm.nih.gov/36377901
Title of parent work (English):mSystems
Publisher:American Society for Microbiology
Place of publishing:Washington, DC
Publication type:Article
Language:English
Date of first publication:2022/11/15
Publication year:2022
Release date:2024/09/19
Tag:Aral Sea; archaea; bacteria; desiccation; metagenome; microbiome; nutrient cycling; revegetation; soil microorganisms
Volume:7
Issue:6
Number of pages:16
Organizational units:Mathematisch-Naturwissenschaftliche Fakultät / Institut für Biochemie und Biologie
DDC classification:5 Naturwissenschaften und Mathematik / 57 Biowissenschaften; Biologie / 570 Biowissenschaften; Biologie
Peer review:Referiert
Publishing method:Open Access / Gold Open-Access
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License (German):License LogoCC-BY - Namensnennung 4.0 International
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