Genome-resolved Metagenomics Identifies the Particular Genetic Traits of Phosphate-solubilizing Bacteria in Agricultural Soil

Overview

Journal ISME Commun

Publisher Oxford University Press

Date 2023 Nov 8

PMID 37938650

Authors

Xingjie Wu

Zhenling Cui

Jingjing Peng

Fusuo Zhang

Werner Liesack

Affiliations

Soon will be listed here.

Abstract

Bacteria play a key role in phosphate solubilization, but related genome-centric research on agricultural microbiomes is scarce. Here, we reconstructed 472 metagenome-assembled genomes (MAGs) covering agricultural soils from six long-term field trials across China. A total of 79 MAGs contained gcd encoding quinoprotein glucose dehydrogenase (GCD), which is the key biomarker for phosphate solubilization. Our findings showed that all GCD-MAGs represent potentially novel species, with gcd copy numbers varying from 1 to 10 per genome. Large genome size, a high ratio of glycosyl hydrolase genes, and increased capacity for carbohydrate utilization were specific traits of GCD-MAGs. Notably, the gcd copy number showed a significant and positive correlation with genome size. Generated using a machine learning approach, our findings were validated in a dataset of 692 genotypes covering the 18 bacterial families to which the 79 GCD-MAGs belong. Our results improve the knowledge of both the diversity and the genetic composition of phosphate-solubilizing bacteria. In particular, they reveal a genomic link between phosphate solubilization capacity and increased potential for carbohydrate metabolism, which may accelerate targeted engineering and improve management practices for sustainable agriculture.

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References

Li J, Lu J, Wang H, Fang Z, Wang X, Feng S . A comprehensive synthesis unveils the mysteries of phosphate-solubilizing microbes. Biol Rev Camb Philos Soc. 2021; 96(6):2771-2793. PMC: 9291587. DOI: 10.1111/brv.12779. View

Farhat M, Boukhris I, Chouayekh H . Mineral phosphate solubilization by Streptomyces sp. CTM396 involves the excretion of gluconic acid and is stimulated by humic acids. FEMS Microbiol Lett. 2015; 362(5). DOI: 10.1093/femsle/fnv008. View

Mogollon J, Bouwman A, Beusen A, Lassaletta L, van Grinsven H, Westhoek H . More efficient phosphorus use can avoid cropland expansion. Nat Food. 2023; 2(7):509-518. DOI: 10.1038/s43016-021-00303-y. View

Oliverio A, Bissett A, McGuire K, Saltonstall K, Turner B, Fierer N . The Role of Phosphorus Limitation in Shaping Soil Bacterial Communities and Their Metabolic Capabilities. mBio. 2020; 11(5). PMC: 7593963. DOI: 10.1128/mBio.01718-20. View

Hessen D, Jeyasingh P, Neiman M, Weider L . Genome streamlining and the elemental costs of growth. Trends Ecol Evol. 2009; 25(2):75-80. DOI: 10.1016/j.tree.2009.08.004. View

Liang J, Liu J, Jia P, Yang T, Zeng Q, Zhang S . Novel phosphate-solubilizing bacteria enhance soil phosphorus cycling following ecological restoration of land degraded by mining. ISME J. 2020; 14(6):1600-1613. PMC: 7242446. DOI: 10.1038/s41396-020-0632-4. View

Bucking H, Shachar-Hill Y . Phosphate uptake, transport and transfer by the arbuscular mycorrhizal fungus Glomus intraradices is stimulated by increased carbohydrate availability. New Phytol. 2005; 165(3):899-911. DOI: 10.1111/j.1469-8137.2004.01274.x. View

Ye L, Mei R, Liu W, Ren H, Zhang X . Machine learning-aided analyses of thousands of draft genomes reveal specific features of activated sludge processes. Microbiome. 2020; 8(1):16. PMC: 7014675. DOI: 10.1186/s40168-020-0794-3. View

Li J, Mau R, Dijkstra P, Koch B, Schwartz E, Liu X . Predictive genomic traits for bacterial growth in culture versus actual growth in soil. ISME J. 2019; 13(9):2162-2172. PMC: 6776108. DOI: 10.1038/s41396-019-0422-z. View

10.

Willsky G, Bennett R, MALAMY M . Inorganic phosphate transport in Escherichia coli: involvement of two genes which play a role in alkaline phosphatase regulation. J Bacteriol. 1973; 113(2):529-39. PMC: 285262. DOI: 10.1128/jb.113.2.529-539.1973. View

11.

Giovannoni S, Thrash J, Temperton B . Implications of streamlining theory for microbial ecology. ISME J. 2014; 8(8):1553-65. PMC: 4817614. DOI: 10.1038/ismej.2014.60. View

12.

Zhang L, Xu M, Liu Y, Zhang F, Hodge A, Feng G . Carbon and phosphorus exchange may enable cooperation between an arbuscular mycorrhizal fungus and a phosphate-solubilizing bacterium. New Phytol. 2016; 210(3):1022-32. DOI: 10.1111/nph.13838. View

13.

Wu X, Rensing C, Han D, Xiao K, Dai Y, Tang Z . Genome-Resolved Metagenomics Reveals Distinct Phosphorus Acquisition Strategies between Soil Microbiomes. mSystems. 2022; 7(1):e0110721. PMC: 8751388. DOI: 10.1128/msystems.01107-21. View

14.

Wanner B . Gene regulation by phosphate in enteric bacteria. J Cell Biochem. 1993; 51(1):47-54. DOI: 10.1002/jcb.240510110. View

15.

Dai Z, Liu G, Chen H, Chen C, Wang J, Ai S . Long-term nutrient inputs shift soil microbial functional profiles of phosphorus cycling in diverse agroecosystems. ISME J. 2019; 14(3):757-770. PMC: 7031380. DOI: 10.1038/s41396-019-0567-9. View

16.

Yao Q, Li Z, Song Y, Wright S, Guo X, Tringe S . Community proteogenomics reveals the systemic impact of phosphorus availability on microbial functions in tropical soil. Nat Ecol Evol. 2018; 2(3):499-509. DOI: 10.1038/s41559-017-0463-5. View