Abstract
Purpose
Reclamation of saline-alkali soils to grow cotton (Gossypium spp.) is very common in the arid Manas River Basin in Northwest China. However, little is known about the degradation potential of soil microbes in reclaimed saline-alkali soils.
Methods
Hence, in this study, the high-throughput metagenomic sequencing was used to assess the degradation potential of soil microbes over seven years after reclamation. Results The results showed that bacteria is the dominant microbial group, and Actinobacteria, Proteobacteria, Chloroflexi, and Firmicutes were dominant phyla in the soil samples collected in each year. Among them, Actinobacteria and Proteobacteria accounted for more than 60% of the total bacteria. Further, soil microbial diversity and abundance of carbohydrate-active enzymes (CAZymes) encoding genes increased after reclamation, as did the abundance of CAZyme encoding genes involved in the decomposition of cellulose, hemicellulose, chitin, and lignin. Deterministic and stochastic processes jointly dominated the succession of microbial communities in reclaimed soils. Redundancy analysis and permutational multivariate analysis of variance showed that soil EC, C/N ratio, and Na+ content significantly affected microbial community succession and the abundance of CAZyme encoding genes in reclaimed soils, and soil pH affected soil microbial community diversity.
Conclusions
In conclusion, the degradation potential of soil microbes significantly increased after reclamation. This study deepens our understanding of the degradation potential of soil microbes in the process of reclamation of abandoned saline-alkali soils.
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References
Andrade AC, Fróes A, Lopes FÁC, Thompson FL, Krüger RH, Dinsdale E, Bruce T (2017) Diversity of microbial carbohydrate-active enZYmes (CAZYmes) associated with freshwater and soil samples from Caatinga biome. Microb Ecol 74:89–105. https://doi.org/10.1007/s00248-016-0911-9
Berlemont R, Martiny AC (2013) Phylogenetic distribution of potential cellulases in bacteria. Appl Environ Microbiol 79:1545–1554. https://doi.org/10.1128/AEM.03305-12
Berlemont R, Allison SD, Weihe C, Lu Y, Brodie EL, Martiny JB, Martiny AC (2014) Cellulolytic potential under environmental changes in microbial communities from grassland litter. Front Microbiol 5:639. https://doi.org/10.3389/fmicb.2014.00639
Briar SS, Steven JF, Inmyoung P, Johan S, Kate S, Howard F (2011) The distribution of nematodes and soil microbial communities across soil aggregate fractions and farm management systems. Soil Biol Biochem 43:905–914. https://doi.org/10.1016/j.soilbio.2010.12.017
Buscardo E, Souza RC, Meir P, Geml J, Schmidt SK, Da Costa AC, Nagy L (2021) Effects of natural and experimental drought on soil fungi and biogeochemistry in an Amazon rain forest. Commun Earth Environ 2:1–12. https://doi.org/10.1038/s43247-021-00124-8
Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37:233–238. https://doi.org/10.1093/nar/gkn663
Cardenas E, Kranabetter JM, Hope G, Maas KR, Hallam S, Mohn WW (2015) Forest harvesting reduces the soil metagenomic potential for biomass decomposition. ISME J 9:2465–2476. https://doi.org/10.1038/ismej.2015.57
Chávez-Romero Y, Navarro-Noya YE, Reynoso-Martínez SC, Sarria-Guzmán Y, Govaerts B, Verhulst N, Dendooven L, Luna-Guido M (2016) 16S metagenomics reveals changes in the soil bacterial community driven by soil organic C, N-fertilizer and tillage-crop residue management. Soil till Res 159:1–8. https://doi.org/10.1016/j.still.2016.01.007
Chen C, Yuan C, Cui J (2019a) Study on Improvement Effect of Saline-alkali Soil by Cationic Modified Biochar. IOP Conf Ser: Earth Environ Sci 310:42–46. https://doi.org/10.1088/1755-1315/310/4/042046
Chen JH, Wu QF, Li SH, Ge JF, Liang CF, Qin H, Xu QF, Fuhrmann JJ (2019b) Diversity and function of soil bacterial communities in response to long-term intensive management in a subtropical bamboo forest. Geoderma 354:113894. https://doi.org/10.1016/j.geoderma.2019.113894
Chen W, Ren K, Isabwe A, Chen H, Liu M, Yang J (2019c) Stochastic processes shape microeukaryotic community assembly in a subtropical river across wet and dry seasons. Microbiome 7:1–16. https://doi.org/10.1186/s40168-019-0749-8
Cheng ZB, Zhang FH, Gale WJ, Wang WC, Sang W, Yang HC (2017) Effects of reclamation years on composition and diversity of soil bacterial communities in Northwest China. Can J Microbiol 64:28–40. https://doi.org/10.1139/cjm-2017-0362
Cheng Z, Chen Y, Zhang F (2018) Effect of reclamation of abandoned salinized farmland on soil bacterial communities in arid northwest China. Sci Total Environ 630:799–808. https://doi.org/10.1016/j.scitotenv.2018.02.259
Cheng Z, Chen Y, Zhang FH (2019) Effect of cropping systems after abandoned salinized farmland reclamation on soil bacterial communities in arid northwest China. Soil till Res 187:204–213. https://doi.org/10.1016/j.still.2018.12.015
Collins AL, Burak E, Harris P, Pulley S, Cardenas L, Tang Q (2019) Field scale temporal and spatial variability of δ13C, δ15N, TC and TN soil properties: implications for sediment source tracing. Geoderma 333:108–122. https://doi.org/10.1016/j.geoderma.2018.07.019
De Vries M, Schöler A, Ertl J, Xu Z, Schloter M (2015) Metagenomic analyses reveal no differences in genes involved in cellulose degradation under different tillage treatments. FEMS Microbiol Ecol 91:069. https://doi.org/10.1093/femsec/fiv069
Dini-Andreote F, Stegen JC, Van Elsas JD, Salles JF (2015) Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession. P Natl A Sc 112:1326–1332. https://doi.org/10.1073/pnas.1414261112
Egamberdieva D, Renella G, Wirth S, Islam R (2010) Secondary salinity effects on soil microbial biomass. Biol Fert Soils 46:445–449. https://doi.org/10.1007/s00374-010-0452-1
Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. P Natl Acad Sci USA 103:626–631. https://doi.org/10.1073/pnas.0507535103
Gabhane J, William PS, Bidyadhar R, Bhilawe P, Anand D, Vaidya AN, Wate SR (2012) Additives aided composting of green waste: effects on organic matter degradation, compost maturity, and quality of the finished compost. Bioresour Technol 114:382–388. https://doi.org/10.1016/j.biortech.2012.02.040
Glass NL, Schmoll M, Cate JH, Coradetti S (2013) Plant cell wall deconstruction by ascomycete fungi. Annual Rev Microbiol 67:477–498. https://doi.org/10.1146/annurev-micro-092611-150044
Granja-Travez RS, Wilkinson RC, Persinoti GF, Squina FM, Fülöp V, Bugg TD (2018) Structural and functional characterisation of multi-copper oxidase CueO from lignin-degrading bacterium Ochrobactrum sp. reveal its activity towards lignin model compounds and lignosulfonate. FEBS J 285:1684–1700. https://doi.org/10.1111/febs.14437
Himmel ME, Xu Q, Luo Y, Ding SY, Lamed R, Bayer EA (2010) Microbial enzyme systems for biomass conversion: emerging paradigms. Biofuels 1:323–341. https://doi.org/10.4155/bfs.09.25
Knight R, Vrbanac A, Taylor BC, Aksenov A, Callewaert C, Debelius J, Dorrestein PC (2018) Best practices for analysing microbiomes. Nat Rev Microbiol 16:410–422. https://doi.org/10.1038/s41579-018-0029-9
Koeck DE, Pechtl A, Zverlov VV, Schwarz WH (2014) Genomics of cellulolytic bacteria. Curr Opin Biotech 29:171–183. https://doi.org/10.3389/fmicb.2017.00644
Kunath BJ, Bremges A, Weimann A, McHardy AC, Pope PB (2017) Metagenomics and CAZyme discovery. In Protein-Carbohydrate Interactions. Humana Press, New York, pp 255–277. https://doi.org/10.1007/978-1-4939-6899-2_20
Li J, Pu L, Han M, Zhu M, Zhang R, Xiang Y (2014) Soil salinization research in China: advances and prospects. J Geogr Sci 24:943–960. https://doi.org/10.1007/s11442-014-1130-2
Li S, Li Y, Hu C, Zheng X, Zhang J, Zhang H, Lv W (2021) Stochastic processes drive bacterial and fungal community assembly in sustainable intensive agricultural soils of Shanghai, China. Sci Total Environ 778:146021. https://doi.org/10.1016/j.scitotenv.2021.146021
Lin YX, Ye GP, Kuzyakov Y, Liu DY, Fan JB, Ding WX (2019) Long-term manure application increases soil organic matter and aggregation, and alters microbial community structure and keystone taxa. Soil Biol Biochem 134:187–196. https://doi.org/10.1016/j.soilbio.2019.03.030
Liu J, Sui Y, Yu Z, Shi Y, Chu H, Jin J, Liu X, Wang G (2014) High throughput sequencing analysis of biogeographical distribution of bacterial communities in the black soils of northeast China. Soil Biol Biochem 70:113–122. https://doi.org/10.1016/j.soilbio.2013.12.014
Liu W, Graham EB, Dong Y, Zhong L, Zhang J, Qiu C, Feng Y (2021) Balanced stochastic versus deterministic assembly processes benefit diverse yet uneven ecosystem functions in representative agroecosystems. Environ Microbiol 23:391–404. https://doi.org/10.1111/1462-2920.15326
Lombard V, Ramulu HG, Drula E, Coutinho PM, Henrissat B (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42:490–495. https://doi.org/10.1093/nar/gkt1178
López-Mondéjar R, Zühlke D, Becher D, Riedel K, Baldrian P (2016) Cellulose and hemicellulose decomposition by forest soil bacteria proceeds by the action of structurally variable enzymatic systems. Sci Rep-UK 6:1–12. https://doi.org/10.1038/srep25279
Luo S, Wang S, Tian L, Shi S, Xu S, Yang F, Li XJ, Wang ZC, Tian CJ (2018) Aggregate-related changes in soil microbial communities under different ameliorant applications in saline-sodic soils. Geoderma 329:108–117. https://doi.org/10.1016/j.geoderma.2018.05.023
Ma CF, Lo PK, Xu JQ, Li MQ, Jiang ZW, Li G, Zhu QH, Li XT, Leong SY, Li QL (2020) Molecular mechanisms underlying lignocellulose degradation and antibiotic resistance genes removal revealed via metagenomics analysis during different agricultural wastes composting. Bioresource Technol 314:123731. https://doi.org/10.1016/j.biortech.2020.123731
Macêdo WV, Sakamoto IK, Azevedo EB, Damianovic MHR (2019) The effect of cations (Na+, Mg2+, and Ca2+) on the activity and structure of nitrifying and denitrifying bacterial communities. Sci Total Environ 679:279–287. https://doi.org/10.1016/j.scitotenv.2019.04.397
Moorhead DL, Sinsabaugh RL (2006) A theoretical model of litter decay and microbial interaction. Ecol Monogr 76:151–174. https://doi.org/10.1890/0012-9615(2006)076
Neupane S, Goyer C, Zebarth BJ, Li S, Whitney S (2019) Soil bacterial communities exhibit systematic spatial variation with landform across a commercial potato field. Geoderma 335:112–122. https://doi.org/10.1016/j.geoderma.2018.08.016
Oh HN, Park D, Seong HJ, Kim D, Sul WJ (2019) Antarctic tundra soil metagenome as useful natural resources of cold-active lignocelluolytic enzymes. J Microbiol 57:865–873. https://doi.org/10.1007/s12275-019-9217-1
Oren A (2008) Microbial life at high salt concentrations: phylogenetic and metabolic diversity. Saline Syst 4:1–13. https://doi.org/10.1186/1746-1448-4-2
Palomo A, Fowler SJ, Gülay A, Rasmussen S, Sicheritz-Ponten T, Smets BF (2016) Metagenomic analysis of rapid gravity sand filter microbial communities suggests novel physiology of Nitrospira spp. ISME J 10:2569–2581. https://doi.org/10.1038/ismej.2016.63
Park BH, Karpinets TV, Syed MH, Leuze MR, Uberbacher EC (2010) CAZymes Analysis Toolkit (CAT): web service for searching and analyzing carbohydrate-active enzymes in a newly sequenced organism using CAZy database. Glycobiology 20:1574–1584. https://doi.org/10.1093/glycob/cwq106
Rath KM, Fierer N, Murphy DV, Rousk J (2019) Linking bacterial community composition to soil salinity along environmental gradients. ISME J 13:836–846. https://doi.org/10.1038/s41396-018-0313-8
Rukhovich DI, Simakova MS, Kulyanitsa AL, Bryzzhev AV, Koroleva PV, Kalinina NV, Rukhovich SV (2017) The influence of soil salinization on land use changes in azov district of Rostov oblast. Eurasian Soil Sci 50:276–295. https://doi.org/10.1134/s1064229317010136
Salam LB (2018) Detection of carbohydrate-active enzymes and genes in a spent engine oil-perturbed agricultural soil. Bull Natl Res Cent 42:1–18. https://doi.org/10.1186/s42269-018-0013-6
Shen CC, Shi Y, Fan KK, He JS, Adams JM, Ge Y, Chu HY (2019) Soil pH dominates elevational diversity pattern for bacteria in high elevation alkaline soils on the Tibetan Plateau. FEMS Microbiol Ecol 95:003. https://doi.org/10.1093/femsec/fiz003
Shi Y, Liu X, Zhang Q, Gao P, Ren J (2020) Biochar and organic fertilizer changed the ammonia-oxidizing bacteria and archaea community structure of saline–alkali soil in the North China Plain. J Soil Sediment 20:12–23. https://doi.org/10.1007/s11368-019-02364-w
Šnajdr J, Cajthaml T, Valášková V, Merhautová V, Petránková M, Spetz P, Kaisu L, Baldrian P (2011) Transformation of Quercus petraea litter: successive changes in litter chemistry are reflected in differential enzyme activity and changes in the microbial community composition. FEMS Microbiol Ecol 75:291–303. https://doi.org/10.1111/j.1574-6941.2010.00999.x
Solans M, Vobis G (2003) Saprophytic actinomycetes associated to the rhizosphere and rhizoplane of Discaria trinervis. Ecol Austral 13:97–107
Su JQ, Wei B, Ouyang WY, Huang FY, Zhao Y, Xu HJ, Zhu YG (2015) Antibiotic resistome and its association with bacterial communities during sewage sludge composting. Environ Sci Technol 49:7356–7363. https://doi.org/10.1021/acs.est.5b01012
Syed K, Doddapaneni H, Subramanian V, Lam YW, Yadav JS (2010) Genome-to-function characterization of novel fungal P450 monooxygenases oxidizing polycyclic aromatic hydrocarbons (PAHs). Biochem Bioph Res Co 399:492–497. https://doi.org/10.1016/j.bbrc.2010.07.094
Tian M, Du D, Zhou W, Zeng X, Cheng G (2017) Phenol degradation and genotypic analysis of dioxygenase genes in bacteria isolated from sediments. Braz J Microbiol 48:305–313. https://doi.org/10.1016/j.bjm.2016.12.002
Trego AC, McAteer PG, Nzeteu C, Mahony T, Abram F, Ijaz UZ, O’Flaherty V (2021) Combined stochastic and deterministic processes drive community assembly of anaerobic microbiomes during granule flotation. Front Microbiol 12:1165. https://doi.org/10.3389/fmicb.2021.666584
Uroz S, Ioannidis P, Lengelle J, Cébron A, Morin E, Buee M, Martin F (2013) Functional assays and metagenomic analyses reveals differences between the microbial communities inhabiting the soil horizons of a Norway spruce plantation. PLoS ONE 8:e55929. https://doi.org/10.1371/journal.pone.0055929
Verzeaux J, Alahmad A, Habbib H (2016) Cover crops prevent the deleterious effect of nitrogen fertilisation on bacterial diversity by maintaining the carbon content of ploughed soil. Geoderma 281:49–57. https://doi.org/10.1016/j.geoderma.2016.06.035
Wang M, Chen S, Chen L, Wang D (2019) Responses of soil microbial communities and their network interactions to saline-alkaline stress in Cd-contaminated soils. Environ Pollut 252:1609–1621. https://doi.org/10.1016/j.envpol.2019.06.082
Wang J, Long Z, Min W, Hou Z (2020a) Metagenomic analysis reveals the effects of cotton straw–derived biochar on soil nitrogen transformation in drip-irrigated cotton field. Environ Sci Pollut R 27:43929–43941. https://doi.org/10.1007/s11356-020-10267-4
Wang Y, Liu L, Yang J, Duan Y, Luo Y, Taherzadeh MJ, Li YF, Li HK, Awasthi MK, Zhao Z (2020b) The diversity of microbial community and function varied in response to different agricultural residues composting. Sci Total Environ 715:136983. https://doi.org/10.1016/j.scitotenv.2020.136983
Wei H, Wang L, Hassan M, Xie B (2018) Succession of the functional microbial communities and the metabolic functions in maize straw composting process. Bioresource Technol 256:333–341. https://doi.org/10.1016/j.biortech.2018.02.050
Wu C, Yin Y, Yang X, Feng L, Tang H, Tao J (2019) A Markov-based model for predicting the development trend of soil microbial communities in saliane-alkali land in Wudi County. Concurr Comp-Pract E 31:4754. https://doi.org/10.1002/cpe.4754
Wu H, Tang T, Zhu F, Wei X, Hartley W, Xue S (2021) Long term natural restoration creates soil-like microbial communities in bauxite residue: A 50-year filed study. Land Degrad Dev 32:1606–1617. https://doi.org/10.1002/ldr.3728
Yang L, Tan L, Zhang F, Gale WJ, Cheng Z, Sang W (2018) Duration of continuous cropping with straw return affects the composition and structure of soil bacterial communities in cotton fields. Can J Microbiol 64:167–181. https://doi.org/10.1139/cjm-2017-0443
Yang X, Zhu K, Loik ME, Sun W (2021) Differential responses of soil bacteria and fungi to altered precipitation in a meadow steppe. Geoderma 384:114812. https://doi.org/10.1016/j.geoderma.2020.114812
Yin F, Zhang F, Wang H (2021) Rhizosphere bacteria community and functions under typical natural halophyte communities in North China salinized areas. PLoS ONE 16:e0259515. https://doi.org/10.1371/journal.pone.0259515
Yip VL, Withers SG (2006) Breakdown of oligosaccharides by the process of elimination. Curr Opin Chem Biol 10:147–155. https://doi.org/10.1016/j.cbpa.2006.02.005
Yu LH, Wu SJ, Peng YS, Liu RN, Chen X, Zhao P, Xu P, Zhu JB, Jiao GL, Pei Y, Xiang CB (2016) Arabidopsis EDT1/HDG11 improves drought and salt tolerance in cotton and poplar and increases cotton yield in the field. Plant Biotechnol J 14:72–84. https://doi.org/10.1111/pbi.12358
Zhang W, Du Y (2018) Analysis of the succession of structure of the bacteria community in soil from long-term continuous cotton cropping in Xinjiang using high-throughput sequencing. Arch Microbiol 200:653–662. https://doi.org/10.1007/s00203-018-1476-4
Zhang KR, Cheng XL, Shu X, Liu Y, Zhang QF (2018) Linking soil bacterial and fungal communities to vegetation succession following agricultural abandonment. Plant Soil 431:19–36. https://doi.org/10.1007/s11104-018-3743-1
Zhang K, Shi Y, Cui X, Yue P, Li K, Liu X, Tripathi BM, Chu H (2019) Salinity is a key determinant for soil microbial communities in a desert ecosystem. Msystems 4:e00225-e318. https://doi.org/10.1128/mSystems.00225-18
Zhang Z, Liu H, Liu X, Chen Y, Lu Y, Shen M, Li J (2022) Organic fertilizer enhances rice growth in severe saline–alkali soil by increasing soil bacterial diversity. Soil Use Manage 38:964–977. https://doi.org/10.1111/sum.12711
Zhao J, Zhang RF, Xue C, Xun WB, Sun Li XuYC, Shen QR (2014) Pyrosequencing reveals contrasting soil bacterial diversity and community structure of two main Winter wheat cropping systems in China. Microb Ecol 67:443–453. https://doi.org/10.1007/s00248-013-0322-0
Zhao Y, Zhang F, Yang L, Wang D, Wang W (2019) Response of soil bacterial community structure to different reclamation years of abandoned salinized farmland in arid China. Arch Microbiol 201:1219–1232. https://doi.org/10.1007/s00203-019-01689-x
Zheng W, Zhao ZY, Lv FL, Wang R, Gong QL, Zhai BN, Wang ZH, Zhao ZY, Li ZY (2019) Metagenomic exploration of the interactions between N and P cycling and SOM turnover in an apple orchard with a cover crop fertilized for 9 years. Biol Fert Soils 55:365–381. https://doi.org/10.1007/s00374-019-01356-9
Zhong Y, Yan W, Wang R, Wang W, Shang GZ (2018) Decreased occurrence of carbon cycle functions in microbial communities along with long-term secondary succession. Soil Biol Biochem 123:207–217. https://doi.org/10.1016/j.soilbio.2018.05.017
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This research was financially supported by the Major Program of Xinjiang Province (grant number: 2018AA005), and the International Science & Technology Cooperation Program of Xinjiang Province (grant number: 2020BC001).
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Yin, F., Zhang, F. Reclamation of abandoned saline-alkali soil increased soil microbial diversity and degradation potential. Plant Soil 477, 521–538 (2022). https://doi.org/10.1007/s11104-022-05451-z
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DOI: https://doi.org/10.1007/s11104-022-05451-z