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2023 Vol.56, Issue 4 Preview Page

Original research article

Comparative Analysis of Microbial Community Characteristic of Acidic and Neutral Soils in Korean Orchards
Do-Hyun Kim1
,
Ji Yong Moon2
,
Soo Young Hong3
,
Hyeonmo Ahn4
,
Yeo Wook Yoon5
,
Hyo Jin Kim6
,
So Youn Lee7
,
Ji Won Kim8
,
Eun-heui Han9
,
Sang Yoon Kim10
,
Eunjin Lee11
,
Hang-Yeon Weon12*
,
Ho-Jong Ju13*
1Researcher, Agricultural Microbiology Division, Department of Agricultural Biology, National Institute of Agricultural Sciences, RDA, Wanju 55365, Korea
2Researcher, Organic Microorganism Research Center, Gyeonggi-do Agricultural Research & Extension Services (ARES), Hwaseong 18388, Korea
3Researcher, Agricultural Environmental Research Section, Gangwon-do ARES, Chuncheon 24203, Korea
4Researcher, Division of Agricultural Environment Research, Chungcheongbuk-do ARES, Cheongju 28130, Korea
5Researcher, Environmentally Friendly Agriculture Division, Chungcheongnam-do ARES, Yesan 32418, Korea
6Researcher, Agricultural Environment Division, Jeollabuk-do ARES, Iksan 54591, Korea
7Researcher, Environment-Friendly agricultural Research Institute, Jeollanam-do ARES, Naju 58213, Korea
8Ph.D. Researcher, Division of Agricultural Environment Research, Gyeongsangbuk-do ARES, Daegu 41404, Korea
9Researcher, Environmental Agriculture Research Department, Gyeongsangnam-do ARES, Jinju 52733, Korea
10Professor, Department of Agricultural Chemistry & Interdisciplinary Program in IT-Bio Convergence System, Sunchon National University, Sunchon 57922, Korea
11Ph.D. Researcher, Soil and Fertilizer Division, Department of Agricultural Environment, National Institute of Agricultural Sciences, RDA, Wanju 55365, Korea
12Ph.D. Researcher, Agricultural Microbiology Division, Department of Agricultural Biology, National Institute of Agricultural Sciences, RDA, Wanju 55365, Korea
13Professor, Department of Agricultural Biology, College of Agricultural and Life Science, Jeonbuk National University, Jeonju 54896, Korea
*Corresponding Author
30 November 2023. pp. 449-462
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Abstract

Soil microorganism is one of the most important factors in evaluating and improving soil quality because they play a crucial role in the soil material circulation. They are closely correlated with soil environmental factors, and in particular, soil pH has a significant impact on the microbial community. This study aimed to examine the relationship between microbial communities and soil pH in orchard soil of the Republic of Korea. Microbial communities of 63 sites with neutral soil pH (pH 6 - 7) and 26 sites with acidic soil pH (pH 3 - 5) were analyzed targeting 16S rRNA and ITS genes through Illumina Miseq platform. Our analyses showed that bacterial richness and diversity and fungal richness in neutral soil were significantly higher than those in acidic soil (p < 0.001). According to PCoA and PERMANOVA, the microbial communities were significantly different in two soil groups, and ANCOM-BC showed high abundance of 16 bacterial and 15 fungal genera in neutral soil. Lastly, 9 genera, including Terrimonas, Povalibacter and Gp taxa, were identified as hub genera that have a significant impact on other microbial taxa in neutral soil. These results indicated that soil pH is a critical determinant of microbial communities and can serve as an indicator soil quality monitoring and evaluation.

Network analysis to discover hub genera of bacteria (A) and fungi (B) in soil with two pH ranges.
Keywords
Microbial network
Soil microorganisms
Soil quality indicator
References
1
Al-Taai, S.H.H. 2021. Soil pollution-causes and effects. IOP Conf. Ser.: Earth Environ. Sci. 790:012009. 10.1088/1755-1315/790/1/012009
2
Aziz, I., T. Mahmood, and K.R. Islam. 2013. Effect of long term no-till and conventional tillage practices on soil quality. Soil Tillage Res. 131:28-35. 10.1016/j.still.2013.03.002
3
Bais, H.P., T.L. Weir, L.G. Perry, S. Gilroy, and J.M. Vivanco. 2006. The role of root exudates in rhizosphere interactions with plants and other organisms. Annu. Rev. Plant Biol. 57:233-266. 10.1146/annurev.arplant.57.032905.10515916669762
4
Bakker, M.G., J.M. Chaparro, D.K. Manter, and J.M. Vivanco. 2015. Impacts of bulk soil microbial community structure on rhizosphere microbiomes of Zea mays. Plant Soil 392:115-126. 10.1007/s11104-015-2446-0
5
Banerjee, S., K. Schlaeppi, and M.G. van der Heijden. 2018. Keystone taxa as drivers of microbiome structure and functioning. Nat. Rev. Microbiol. 16:567-576. 10.1038/s41579-018-0024-129789680
6
Bartram, A.K., X. Jiang, M.D. Lynch, A.P. Masella, G.W. Nicol, J. Dushoff, and J.D. Neufeld. 2014. Exploring links between pH and bacterial community composition in soils from the Craibstone Experimental Farm. FEMS Microbiol. Ecol. 87:403-415. 10.1111/1574-6941.1223124117982
7
Bohlool, B.B., J.K. Ladha, D.P. Garrity, and T. George. 1992. Biological nitrogen fixation for sustainable agriculture: A perspective. Plant Soil 141:1-11. 10.1007/BF00011307
8
Bonacich, P. 2007. Some unique properties of eigenvector centrality. Soc. Networks 29:555-564. 10.1016/j.socnet.2007.04.002
9
Brimecombe, M.J., F.A. De Leij, and J.M. Lynch. 2000. The effect of root exudates on rhizosphere microbial populations. p. 95-140. In R. Pinton et al. (ed.) The rhizosphere: Biochemistry and organic substances at the soil-plant interface. CRC Press, Boca Raton, FL, USA.
10
Cha, J.Y., S. Han, H.J. Hong, H. Cho, D. Kim, Y. Kwon, S.K. Kwon, M. Crüsemannr, Y.B. Lee, J.F. Kim, G. Giaever, C. Nislow, B.S. Moore, L.S. Thomashow, D.M. Weller, and Y.S. Kwak. 2016. Microbial and biochemical basis of a Fusarium wilt-suppressive soil. ISME J. 10:119-129. 10.1038/ismej.2015.9526057845PMC4681868
11
Chodak, M., M. Gołębiewski, J. Morawska-Płoskonka, K. Kuduk, and M. Niklińska. 2015. Soil chemical properties affect the reaction of forest soil bacteria to drought and rewetting stress. Ann. Microbiol. 65:1627-1637. 10.1007/s13213-014-1002-026273241PMC4529456
12
Compant, S., M.G. Van Der Heijden, and A. Sessitsch. 2010. Climate change effects on beneficial plant-microorganism interactions. FEMS Microbiol. Ecol. 73:197-214. 10.1111/j.1574-6941.2010.00900.x20528987
13
Constancias, F., S. Terrat, N.P. Saby, W. Horrigue, J. Villerd, J.P. Guillemin, L. Biju-Duval, V. Nowak, S. Dequiedt, L. Ranjard, and N.C. Prévost-Bouré. 2015. Mapping and determinism of soil microbial community distribution across an agricultural landscape. MicrobiologyOpen 4:505-517. 10.1002/mbo3.25525833770PMC4475391
14
Dewen, Q., D. Yijie, Z. Yi, L. Shupeng, and S. Fachao. 2017. Plant immunity inducer development and application. Mol. Plant-Microbe Interact. 30:355-360. 10.1094/MPMI-11-16-0231-CR28323528
15
Edgar, R.C. 2013. UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10:996-998. 10.1038/nmeth.260423955772
16
Fierer, N. 2017. Embracing the unknown: Disentangling the complexities of the soil microbiome. Nat. Rev. Microbiol. 15:579-590. 10.1038/nrmicro.2017.8728824177
17
Fierer, N. and R.B. Jackson. 2006. The diversity and biogeography of soil bacterial communities. Proc. Natl. Acad. Sci. 103:626-631. 10.1073/pnas.050753510316407148PMC1334650
18
Fierer, N., M.A. Bradford, and R.B. Jackson. 2007. Toward an ecological classification of soil bacteria. Ecology 88:1354-1364. 10.1890/05-183917601128
19
Goulding, K.W.T. 2016. Soil acidification and the importance of liming agricultural soils with particular reference to the United Kingdom. Soil Use Manage. 32:390-399. 10.1111/sum.1227027708478PMC5032897
20
Hemkemeyer, M., S.A. Schwalb, S. Heinze, R.G. Joergensen, and F. Wichern. 2021. Functions of elements in soil microorganisms. Microbiol. Res. 252:126832. 10.1016/j.micres.2021.12683234508963
21
Hermans, S.M., H.L. Buckley, B.S. Case, F. Curran-Cournane, M. Taylor, and G. Lear. 2017. Bacteria as emerging indicators of soil condition. Appl. Environ. Microbiol. 83:e02826-16. 10.1128/AEM.02826-1627793827PMC5165110
22
Karimi, B., S. Dequiedt, S. Terrat, C. Jolivet, D. Arrouays, P. Wincker, C. Cruaud, A. Bisop, N.C. Prévost-Bouré, and L. Ranjard. 2019. Biogeography of soil bacterial networks along a gradient of cropping intensity. Sci. Rep. 9:3812. 10.1038/s41598-019-40422-y30846759PMC6405751
23
Khan, K.S., R. Mack, X. Castillo, M. Kaiser, and R.G. Joergensen. 2016. Microbial biomass, fungal and bacterial residues, and their relationships to the soil organic matter C/N/P/S ratios. Geoderma 271:115-123. 10.1016/j.geoderma.2016.02.019
24
Kibbey, H.J., C. Hagedorn, and E.L. McCoy. 1978. Use of fecal streptococci as indicators of pollution in soil. Appl. Environ. Microbiol. 35:711-717. 10.1128/aem.35.4.711-717.1978417673PMC242911
25
Kim, H.S., S.H. Lee, H.Y. Jo, K.T. Finneran, and M.J. Kwon. 2021. Diversity and composition of soil Acidobacteria and Proteobacteria communities as a bacterial indicator of past land-use change from forest to farmland. Sci. Total Environ. 797:148944. 10.1016/j.scitotenv.2021.14894434298360
26
Kim, J.M., A.S. Roh, S.C. Choi, E.J. Kim, M.T. Choi, B.K. Ahn, S.K. Kim, Y.H. Lee, J.H. Joa, S.S. Kang, S.A. Lee, J.H. Ahn, J. Song, and H.Y. Weon. 2016. Soil pH and electrical conductivity are key edaphic factors shaping bacterial communities of greenhouse soils in Korea. J. Microbiol. 54:838-845. 10.1007/s12275-016-6526-527888456
3
Kim, J.W., Y.K. Hong, C.R. Lee, and S.C. Kim. 2023. Comparison of physicochemical and biological soil properties in organic and conventional upland fields. Korean J. Soil Sci. Fert. 56:77-89. 10.7745/KJSSF.2023.56.1.077
28
Lamb, E.G., N. Kennedy, and S.D. Siciliano. 2011. Effects of plant species richness and evenness on soil microbial community diversity and function. Plant Soil 338:483-495. 10.1007/s11104-010-0560-6
29
Lauber, C.L., M. Hamady, R. Knight, and N. Fierer. 2009. Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl. Environ. Microbiol. 75:5111-5120. 10.1128/AEM.00335-0919502440PMC2725504
30
Läuchli, A. and S.R. Grattan. 2012. Soil pH extremes. p. 194-209. In S. Shabala (ed.) Plant stress physiology. CABI, Wallingford, CT, USA. 10.1079/9781845939953.0194
31
Layeghifard, M., D.M. Hwang, and D.S. Guttman. 2017. Disentangling interactions in the microbiome: A network perspective. Trends Microbiol. 25:217-228. 10.1016/j.tim.2016.11.00827916383PMC7172547
32
Lee, K.K., H. Kim, and Y.H. Lee. 2022. Cross-kingdom co-occurrence networks in the plant microbiome: Importance and ecological interpretations. Front. Microbiol. 13:953300. 10.3389/fmicb.2022.95330035958158PMC9358436
33
Lee, S.A., J.M. Kim, Y. Kim, J.H. Joa, S.S. Kang, J.H. Ahn, M. Kim, J. Song, and H.Y. Weon. 2020. Different types of agricultural land use drive distinct soil bacterial communities. Sci. Rep. 10:17418. 10.1038/s41598-020-74193-833060673PMC7562711
34
Lin, H. and S.D. Peddada. 2020. Analysis of compositions of microbiomes with bias correction. Nat. Commun. 11:3514. 10.1038/s41467-020-17041-732665548PMC7360769
35
Lu, T., N. Xu, C. Lei, Q. Zhang, Z. Zhang, L. Sun, F. He, N.Y. Zhou, J. Peñuelas, Y.G. Zhu, and H. Qian. 2023. Bacterial biogeography in China and its association to land use and soil organic carbon. Soil Ecol. Lett. 5:230172. 10.1007/s42832-023-0172-8
36
Lynch, J.M. and E. Bragg. 1985. Microorganisms and soil aggregate stability. p. 133-171. In B.A. Stewart (ed.) Advances in soil science: Volume 2. Springer, Manhattan, NY, USA. 10.1007/978-1-4612-5088-3_3
37
Mamet, S.D., E. Redlick, M. Brabant, E.G. Lamb, B.L. Helgason, K. Stanley, and S.D. Siciliano. 2019. Structural equation modeling of a winnowed soil microbiome identifies how invasive plants re-structure microbial networks. ISME J. 13:1988-1996. 10.1038/s41396-019-0407-y30926920PMC6776034
38
Marschner, P., D. Crowley, and C.H. Yang. 2004. Development of specific rhizosphere bacterial communities in relation to plant species, nutrition and soil type. Plant Soil 261:199-208. 10.1023/B:PLSO.0000035569.80747.c5
39
Massa, S., G.F. Brocchi, G. Peri, C. Altieri, and C. Mammina. 2001. Evaluation of recovery methods to detect faecal streptococci in polluted waters. Lett. Appl. Microbiol. 32:298-302. 10.1046/j.1472-765X.2001.00904.x11328493
40
Matos, A., L. Kerkhof, and J.L. Garland. 2005. Effects of microbial community diversity on the survival of Pseudomonas aeruginosa in the wheat rhizosphere. Microb. Ecol. 49:257-264. 10.1007/s00248-004-0179-315965723
41
McMurdie, P.J. and S. Holmes. 2013. Phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8:e61217. 10.1371/journal.pone.006121723630581PMC3632530
42
Miltner, A., P. Bombach, B. Schmidt-Brücken, and M. Kästner. 2012. SOM genesis: Microbial biomass as a significant source. Biogeochemistry 111:41-55. 10.1007/s10533-011-9658-z
43
NAAS. 2010. Methods of soil chemical analysis. National Institute of Agricultural Sciences, RDA, Suwon, Korea.
44
Petriglieri, F., M. Nierychlo, P.H. Nielsen, and S.J. McIlroy. 2018. In situ visualisation of the abundant Chloroflexi populations in full-scale anaerobic digesters and the fate of immigrating species. PLoS One 13:e0206255. 10.1371/journal.pone.020625530383873PMC6211663
45
Rousk, J., E. Bååth, P.C. Brookes, C.L. Lauber, C. Lozupone, J.G. Caporaso, R. Knight, and N. Fierer. 2010. Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J. 4:1340-1351. 10.1038/ismej.2010.5820445636
46
Schloss, P.D., S.L. Westcott, T. Ryabin, J.R. Hall, M. Hartmann, E.B. Hollister, R.A. Lesniewski, and C.F. Weber. 2009. Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75:7537-7541. 10.1128/AEM.01541-0919801464PMC2786419
47
Schreiter, S., G.C. Ding, H. Heuer, G. Neumann, M. Sandmann, R. Grosch, S. Kropf, and K. Smalla. 2014. Effect of the soil type on the microbiome in the rhizosphere of field-grown lettuce. Front. Microbiol. 5:144. 10.3389/fmicb.2014.0014424782839PMC3986527
48
Siles, J.A. and R. Margesin. 2017. Seasonal soil microbial responses are limited to changes in functionality at two Alpine forest sites differing in altitude and vegetation. Sci. Rep. 7:2204. 10.1038/s41598-017-02363-228526872PMC5438347
49
Sims, J.T. 1986. Soil pH effects on the distribution and plant availability of manganese, copper, and zinc. Soil Sci. Soc. Am. J. 50:367-373. 10.2136/sssaj1986.03615995005000020023x
50
Sørensen, J. 1997. The rhizosphere as a habitat for soil microorganisms. p. 21-45. In J. Dirk van Elsas et al. (ed.) Modern soil microbiology. Marcel Dekker, NY, USA.
51
Tian, D. and S. Niu. 2015. A global analysis of soil acidification caused by nitrogen addition. Environ. Res. Lett. 10:024019. 10.1088/1748-9326/10/2/024019
52
Tisdall, J.M. and J.M. Oades. 1982. Organic matter and water-stable aggregates in soils. J. Soil Sci. 33:141-163. 10.1111/j.1365-2389.1982.tb01755.x
53
Torsvik, V., L. Øvreås, and T.F. Thingstad. 2002. Prokaryotic diversity-magnitude, dynamics, and controlling factors. Science 296:1064-1066. 10.1126/science.107169812004116
54
Tripathi, B.M., J.C. Stegen, M. Kim, K. Dong, J.M. Adams, and Y.K. Lee. 2018. Soil pH mediates the balance between stochastic and deterministic assembly of bacteria. ISME J. 12:1072-1083. 10.1038/s41396-018-0082-429515169PMC5864241
55
Van Donsel, D.J., E.E. Geldreich, and N.A. Clarke. 1967. Seasonal variations in survival of indicator bacteria in soil and their contribution to storm-water pollution. Appl. Microbiol. 15:1362-1370. 10.1128/am.15.6.1362-1370.196716349746PMC547201
56
Vlot, A.C., J.H. Sales, M. Lenk, K. Bauer, A. Brambilla, A. Sommer, Y. Chen, M. Wenig, and S. Nayem. 2021. Systemic propagation of immunity in plants. New Phytol. 229:1234-1250. 10.1111/nph.1695332978988
57
Whitman, W.B., D.C. Coleman, and W.J. Wiebe. 1998. Prokaryotes: The unseen majority. Proc. Natl. Acad. Sci. 95:6578-6583. 10.1073/pnas.95.12.65789618454PMC33863
58
Xu, Q., N. Ling, H. Chen, Y. Duan, S. Wang, Q. Shen, and P. Vandenkoornhuyse. 2020. Long-term chemical-only fertilization induces a diversity decline and deep selection on the soil bacteria. mSystems 5:10-1128. 10.1128/mSystems.00337-2032665327PMC7363003
59
Yoon, J.H., K.H. Kim, and J.E. Yang. 2022. Difference in soil biogeochemical properties of agricultural highland by topographical characteristic and soil management. Korean J. Soil Sci. Fert. 55:1-12. 10.7745/KJSSF.2022.55.1.001
60
Zhao, J., Y. Dong, X. Xie, X. Li, X. Zhang, and X. Shen. 2011. Effect of annual variation in soil pH on available soil nutrients in pear orchards. Acta Ecol. Sin. 31:212-216. 10.1016/j.chnaes.2011.04.001
61
Zhao, W., X. Liu, Q. Huang, and P. Cai. 2015. Streptococcus suis sorption on agricultural soils: Role of soil physico-chemical properties. Chemosphere 119:52-58. 10.1016/j.chemosphere.2014.05.06024968305
Information
  • Publisher :Korean Society of Soil Science and Fertilizer
  • Publisher(Ko) :한국토양비료학회
  • Journal Title :Korean Journal of Soil Science and Fertilizer
  • Journal Title(Ko) :한국토양비료학회 학회지
  • Volume : 56
  • No :4
  • Pages :449-462
  • Received Date : 2023-10-30
  • Revised Date : 2023-11-23
  • Accepted Date : 2023-11-24
  • DOI :https://doi.org/10.7745/KJSSF.2023.56.4.449
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