Reduced trace gas oxidizers as a response to organic carbon ... - Nature.com

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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.

References

  1. Makhalanyane TP, Valverde A, Gunnigle E, Frossard A, Ramond JB, Cowan DA. Microbial ecology of hot desert edaphic systems. FEMS Microbiol Rev. 2015;39:203–21.

    Article  CAS  PubMed  Google Scholar 

  2. Pointing SB, Belnap J. Microbial colonization and controls in dryland systems. Nat Rev Microbiol. 2012;10:551–62.

    Article  CAS  PubMed  Google Scholar 

  3. Ji M, Greening C, Vanwonterghem I, Carere CR, Bay SK, Steen JA, et al. Atmospheric trace gases support primary production in Antarctic desert surface soil. Nature 2017;552:400–3.

    Article  CAS  PubMed  Google Scholar 

  4. Leung PM, Bay SK, Meier DV, Chiri E, Cowan DA, Gillor O, et al. Energetic basis of microbial growth and persistence in desert ecosystems. mSystems 2020;5:e00495–19.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Cordero PRF, Bayly K, Man Leung P, Huang C, Islam ZF, Schittenhelm RB, et al. Atmospheric carbon monoxide oxidation is a widespread mechanism supporting microbial survival. ISME J. 2019;13:2868–81.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Greening C, Carere CR, Rushton-Green R, Harold LK, Hards K, Taylor MC, et al. Persistence of the dominant soil phylum Acidobacteria by trace gas scavenging. Proc Natl Acad Sci USA. 2015;112:10497–502.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Pinske C, McDowall JS, Sargent F, Sawers RG. Analysis of hydrogenase 1 levels reveals an intimate link between carbon and hydrogen metabolism in Escherichia coli K-12. Microbiology 2012;158:856–68.

    Article  CAS  PubMed  Google Scholar 

  8. Bay SK, Waite DW, Dong X, Gillor O, Chown SL, Hugenholtz P, et al. Chemosynthetic and photosynthetic bacteria contribute differentially to primary production across a steep desert aridity gradient. ISME J. 2021;15:3339–56.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Bay SK, Dong X, Bradley JA, Leung PM, Grinter R, Jirapanjawat T, et al. Trace gas oxidizers are widespread and active members of soil microbial communities. Nat Microbiol. 2021;6:246–56.

    Article  CAS  PubMed  Google Scholar 

  10. Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, et al. Persistence of soil organic matter as an ecosystem property. Nature. 2011;478:49–56.

    Article  CAS  PubMed  Google Scholar 

  11. Marschner B, Kalbitz K. Controls of bioavailability and biodegradability of dissolved organic matter in soils. Geoderma. 2003;113:211–35.

    Article  CAS  Google Scholar 

  12. Fanin N, Fromin N, Buatois B, Hättenschwiler S. An experimental test of the hypothesis of non-homeostatic consumer stoichiometry in a plant litter–microbe system. Ecol Lett. 2013;16:764–72.

    Article  PubMed  Google Scholar 

  13. Fierer N, Bradford MA, Jackson RB. Toward an ecological classification of soil bacteria. Ecology. 2007;88:1354–64.

    Article  PubMed  Google Scholar 

  14. Koch AL. Oligotrophs versus copiotrophs. BioEssays. 2001;23:657–61.

    Article  CAS  PubMed  Google Scholar 

  15. Trivedi P, Anderson IC, Singh BK. Microbial modulators of soil carbon storage: integrating genomic and metabolic knowledge for global prediction. Trends Microbiol. 2013;21:641–51.

    Article  CAS  PubMed  Google Scholar 

  16. Greening C, Grinter R. Microbial oxidation of atmospheric trace gases. Nat Rev Microbiol. 2022;20:513–28.

    Article  CAS  PubMed  Google Scholar 

  17. Ochoa-Hueso R, Eldridge DJ, Delgado-Baquerizo M, Soliveres S, Bowker MA, Gross N, et al. Soil fungal abundance and plant functional traits drive fertile island formation in global drylands. J Ecol. 2018;106:242–53.

    Article  CAS  Google Scholar 

  18. Schlesinger WH, Raikes JA, Hartley AE, Cross AE. On the spatial pattern of soil nutrients in desert ecosystems. Ecology 1996;77:1270.

    Article  Google Scholar 

  19. Chen YJ, Neilson JW, Kushwaha P, Maier RM, Barberán A. Life-history strategies of soil microbial communities in an arid ecosystem. ISME J. 2021;15:649–57.

    Article  CAS  PubMed  Google Scholar 

  20. Ding J, Eldridge DJ. The fertile island effect varies with aridity and plant patch type across an extensive continental gradient. Plant Soil. 2021;459:173–83.

    Article  CAS  Google Scholar 

  21. Miao C, Bai Y, Zhang YQ, She W, Liu L, Qiao Y, et al. Interspecific interactions alter plant functional strategies in a revegetated shrub-dominated community in the Mu Us Desert. Ann Bot. 2022;130:149–58.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: high–resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Li D, Liu CM, Luo R, Sadakane K, Lam TW. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics. 2015;31:1674–6.

    Article  CAS  PubMed  Google Scholar 

  25. Steinegger M, Söding J. MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets. Nat Biotechnol. 2017;35:1026–8.

    Article  CAS  PubMed  Google Scholar 

  26. Zhu WH, Lomsadze A, Borodovsky M. Ab initio gene identification in metagenomic sequences. Nucleic Acids Res. 2010;38:e132.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Patro R, Duggal G, Love MI, Irizarry RA, Kingsford C. Salmon provides fast and bias-aware quantification of transcript expression. Nat Methods. 2017;14:417–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res. 2009;37:D233–D238.

    Article  CAS  PubMed  Google Scholar 

  29. Dai ZM, Zang HD, Chen J, Fu YY, Wang XH, Liu HT, et al. Metagenomic insights into soil microbial communities involved in carbon cycling along an elevation climosequences. Environ Microbiol. 2021;23:4631–45.

    Article  CAS  PubMed  Google Scholar 

  30. Donhauser J, Qi WH, Bergk-Pinto B, Frey B. High temperatures enhance the microbial genetic potential to recycle C and N from necromass in high-mountain soils. Glob Change Biol. 2021;27:1365–86.

    Article  Google Scholar 

  31. Liu FT, Kou D, Chen YL, Xue K, Ernakovich JG, Chen LY, et al. Altered microbial structure and function after thermokarst formation. Glob Change Biol. 2021;27:823–35.

    Article  CAS  Google Scholar 

  32. Sun YF, Liu Z, Zhang YQ, Lai ZG, She WW, Bai YX, et al. Microbial communities and their genetic repertoire mediate the decomposition of soil organic carbon pools in revegetation shrublands in a desert in northern China. Eur J Soil Sci. 2020;71:93–105.

    CAS  Google Scholar 

  33. Søndergaard D, Pedersen CNS, Greening C. HydDB: A web tool for hydrogenase classification and analysis. Sci Rep. 2016;6:34212.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Uritskiy GV, DiRuggiero J, Taylor J. MetaWRAP-a flexible pipeline for genome-resolved metagenomic data analysis. Microbiome. 2018;6:158.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015;25:1043–55.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Bowers RM, Kyrpides NC, Stepanauskas R, Harmon-Smith M, Doud D, Reddy TBK, et al. Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea. Nat Biotechnol. 2017;35:725–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Jordaan K, Lappan R, Dong XY, Aitkenhead LJ, Bay SK, Chiri E, et al. Hydrogen-oxidizing bacteria are abundant in desert soils and strongly stimulated by hydration. mSystems. 2020;5:e01131–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Liu YR, Delgado-Baquerizo M, Bi L, Zhu J, He JZ. Consistent responses of soil microbial taxonomic and functional attributes to mercury pollution across China. Microbiome. 2018;6:183.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Roller BRK, Stoddard SF, Schmidt TM. Exploiting rRNA operon copy number to investigate bacterial reproductive strategies. Nat Microbiol. 2016;1:16160.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Botzman M, Margalit H. Variation in global codon usage bias among prokaryotic organisms is associated with their lifestyles. Genome Biol. 2011;12:R109.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Vieira-Silva S, Rocha EPC. The systemic imprint of growth and its uses in ecological (meta) genomics. PLoS Genet. 2010;6:e1000808.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Stoddard SF, Smith BJ, Hein R, Roller BRK, Schmidt TM. rrnDB: improved tools for interpreting rRNA gene abundance in bacteria and archaea and a new foundation for future development. Nucleic Acids Res. 2015;43:D593–D598.

    Article  CAS  PubMed  Google Scholar 

  43. Li H, Yang S, Semenov MV, Yao F, Ye J, Bu RC, et al. Temperature sensitivity of SOM decomposition is linked with a K-selected microbial community. Glob Change Biol. 2021;27:2763–79.

    Article  CAS  Google Scholar 

  44. Zhu YC, Wang LJ, Zhao XY, Lian J, Zhang ZH. Accumulation and potential sources of heavy metals in soils of the Hetao area, Inner Mongolia, China. Pedosphere. 2020;30:244–52.

    Article  CAS  Google Scholar 

  45. Jones DL, Willett VB. Experimental evaluation of methods to quantify dissolved organic nitrogen (DON) and dissolved organic carbon (DOC) in soil. Soil Biol Biochem. 2006;38:991–9.

    Article  CAS  Google Scholar 

  46. Ghani A, Dexter M, Perrott KW. Hot-water extractable carbon in soils: a sensitive measurement for determining impacts of fertilisation, grazing and cultivation. Soil Biol Biochem. 2003;35:1231–43.

    Article  CAS  Google Scholar 

  47. Lappan R, Shelley G, Islam ZF, Leung PM, Lockwood S, Nauer PA, et al. Molecular hydrogen is an overlooked energy source for marine bacteria. bioRxiv. 2022. https://doi.org/10.1101/2022.01.29.478295.

  48. Lauro FM, McDougald D, Thomas T, Williams TJ, Egan S, Rice S, et al. The genomic basis of trophic strategy in marine bacteria. Proc Natl Acad Sci USA. 2009;106:15527–33.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Roller BRK, Schmidt TM. The physiology and ecological implications of efficient growth. ISME J. 2015;9:1481–7.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Berney M, Greening C, Conrad R, Jacobs WR, Cook GM. An obligately aerobic soil bacterium activates fermentative hydrogen production to survive reductive stress during hypoxia. Proc Natl Acad Sci USA. 2014;111:11479–84.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Moxley J, Smith K. Carbon monoxide production and emission by some Scottis...

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