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Reduced trace gas oxidizers as a response to organic carbon availability linked to oligotrophs in desert fertile islands

The ISME Journal volume 17, pages 1257–1266 (2023)Cite this article

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Abstract

Atmospheric trace gases, such as H2 and CO, are important energy sources for microbial growth and maintenance in various ecosystems, especially in arid deserts with little organic substrate. Nonetheless, the impact of soil organic C availability on microbial trace gas oxidation and the underlying mechanisms are unclear at the community level. This study investigated the energy and life-history strategies of soil microbiomes along an organic C gradient inside and out of Hedysarum scoparium islands dispersed in the Mu Us Desert, China. Metagenomic analysis showed that with increasing organic C availability from bare areas into “fertile islands”, the abundance of trace gas oxidizers (TGOs) decreased, but that of trace gas nonoxidizers (TGNOs) increased. The variation in their abundance was more related to labile/soluble organic C levels than to stable/insoluble organic C levels. The consumption rates of H2 and CO confirmed that organic C addition, especially soluble organic C addition, inhibited microbial trace gas oxidation. Moreover, microorganisms with distinct energy-acquiring strategies showed different life-history traits. The TGOs had lower 16 S rRNA operon copy numbers, lower predicted maximum growth rates and higher proportions of labile C degradation genes, implying the prevalence of oligotrophs. In contrast, copiotrophs were prevalent in the TGNOs. These results revealed a mechanism for the microbial community to adapt to the highly heterogeneous distribution of C resources by adjusting the abundances of taxa with distinct energy and life-history strategies, which would further affect trace gas consumption and C turnover in desert ecosystems.

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Fig. 1: Availability and microbial degradablity of soil organic carbon.
Fig. 2: The composition and abundances of genes involved in utilizing organic C and inorganic trace gas energy sources, which were annotated with the KEGG database.
Fig. 3: Spearman’s correlations between energy metabolism genes and soil organic C availability and organic C degradation genes.
Fig. 4: The ex situ H2 and CO oxidation rates of soil samples collected from the CENTRE and OUTSIDE patches at the 0–10 cm depth.
Fig. 5: Microbial groups with different energy strategies.
Fig. 6: The life-history traits of microbial groups with different energy strategies.
Fig. 7: A conceptual infographic of the interactions among soil organic C availability, microbial life-history strategy and microbial energy strategy that induced by shrub fertile islands in desert.

Data availability

The high-throughput sequencing dataset and metagenomic sequencing dataset are available in the National Center for Biotechnology Information (NCBI) Sequence Read Archive (SRA) database with accession number PRJNA859390 and PRJNA909948.

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Acknowledgements

This study was supported by the National Natural Science Foundation Regional Innovation and Development Joint Fund (U21A201208) and National Natural Science Foundation of China (41830755 and 31870476). We thank Yao Liu and Guoqiang Li for statistical analysis procedure, Haoran Sun for technical support. We additionally thank the anonymous reviewers for their helpful suggestions.

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Authors and Affiliations

  1. State Key Laboratory of Crop Stress Biology in Arid Areas, Shaanxi Key Laboratory of Agricultural and Environmental Microbiology, College of Life Sciences, Northwest A&F University, Yangling, Shaanxi, China

    Shuyue Li, Shanshan Yang, Shuo Jiao, Wen Luo, Weimin Chen & Gehong Wei

  2. College of Natural Resources and Environment, Northwest A&F University, Yangling, Shaanxi, China

    Xiaomeng Wei

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  1. Shuyue Li
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Contributions

GW, WC and SL conceived and supervised this study. SL, WC and SY performed field sampling. SL and WL performed bioinformatic analysis. SL performed laboratory work and led the writing of the manuscript. WC, XW, SJ and SL contributed to manuscript revisions.

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Correspondence to Weimin Chen or Gehong Wei.

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Li, S., Yang, S., Wei, X. et al. Reduced trace gas oxidizers as a response to organic carbon availability linked to oligotrophs in desert fertile islands. ISME J 17, 1257–1266 (2023). https://doi.org/10.1038/s41396-023-01437-6

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