Spatial variation of soil bacteria communities and its alpha diversity as a potential bioindicator of land degradation

Authors

  • Muhammad Yusuf Faculty of Mathematics & Natural Sciences, Brawijaya University
  • Adji Ahmad Rinaldo Fernandes Faculty of Mathematics & Natural Sciences, Brawijaya University
  • Syahrul Kurniawan Faculty of Agriculture, Brawijaya University
  • Endang Arisoesilaningsih Faculty of Mathematics & Natural Sciences, Brawijaya University

DOI:

https://doi.org/10.15243/jdmlm.2021.084.2847

Keywords:

alpha diversity, land-use change, soil bacteria community

Abstract

This study aimed at determining the community structure and diversity of soil bacteria in several land-use changes as an environmental bioindicator. This research was conducted in areas of intensive agriculture (PI), monoculture abandoned old-coffee plantation (KTT), mixed-young coffee plantation (HLS), and secondary forest/reference site (RS) in UB Forest (UBF) area, Malang, Indonesia. Soil samples were taken as a composite at three different points in each area using a soil ring at a depth of 0-20 cm. The 16S rRNA gene was used to determine the community structure, species richness, diversity, and ecological index (Chao1, Shannon, Simpson, ACE) of soil bacteria using the NGS approach. Statistical data were analysed using R and QIIME software. The community structure of soil bacteria at the phylum level displayed the same pattern in all study sites where Proteobacteria, Acidobacteria, Actinobacteria, Chloroflexi were the dominant groups. Conversely, the bacterial composition showed differences between study sites at the genus level. Alpha diversity in agricultural areas (PI, KTT, and HLS) was higher than forest area (RS), but it was not followed by bacterial beta diversity. The distinct soil bacteria composition and diversity were influenced by the physicochemical of soil properties in the studied area. Therefore, several bacterial taxa suggested being a potential bioindicator of forest soil degradation due to land-use change in this study. Soil bacterial indicators can be utilized to evaluate or monitor alteration of soil quality in terms of forest restoration or rehabilitation.

References

Bah, A.R. and Rahman, Z.A. 2001. Gliricidia (Gliricidia sepium) Green manures as a potential source of N for maise production in the tropics. The Scientific World Journal 1 Suppl 2: 90-95.

Bárcenas-Moreno, G., Bååth, E., and Rousk, J. 2016. Functional implications of the pH-trait distribution of the microbial community in a re-inoculation experiment across a pH gradient. Soil Biology and Biochemistry 93: 69–78.

Bhatti, A.A., Haq, S. and Bhat, R.A. 2017. Actinomycetes benefaction role in soil and plant health. Microbial Pathogenesis 111: 458-467.

Bissett, A., Richardson, A.E., Baker, G. and Thrall, P.H. 2011. Long-term land use effects on soil microbial community structure and function. Applied Soil Ecology 51(1): 66-78.

Cai, Z. quan, Zhang, Y. hong, Yang, C. and Wang, S. 2018. Land-use type strongly shapes community composition, but not always diversity of soil microbes in tropical China. Catena 165: 369-380.

Caporaso, J.G., Lauber, C.L., Walters, W.A., Berg-Lyons, D., Lozupone, C.A., Turnbaugh, P.J., Fierer, N. and Knight, R. 2011. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proceedings of the National Academy of Sciences of the United States of America 108(Suppl. 1): 4516-4522.

Cho, S.J., Kim, M.H.and Lee, Y.O. 2016. Effect of pH on soil bacterial diversity. Journal of Ecology and Environment 40(1): 1–9.

Cline, L.C. and Zak, D.R. 2015. Soil microbial communities are shaped by plant-driven changes in resource availability during secondary succession. Ecology 96(12): 3374-3385.

Da, E., Jesus, C., Marsh, T.L., Tiedje, J.M., De, F.M. and Moreira, S. 2009. Changes in land use alter the structure of bacterial communities in Western Amazon soils. The ISME Journal 3: 1004-1011.

Delgado-Baquerizo, M., Maestre, F.T., Reich, P.B., Trivedi, P., Osanai, Y., Liu, Y.-R., Hamonts, K., Jeffries, T.C. and Singh, B.K. 2016. Carbon content and climate variability drive global soil bacterial diversity patterns. Ecological Monographs 86(3): 373-390.

Delgado-Baquerizo, M., Reich, P.B., Khachane, A.N., Campbell, C.D., Thomas, N., Freitag, T.E., Abu Al-Soud, W., Sørensen, S., Bardgett, R.D. and Singh, B.K. 2017. It is elemental: soil nutrient stoichiometry drives bacterial diversity. Environmental Microbiology 19(3): 1176-1188.

Dufrene, M. and Legendre, P. 1997. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecological Monographs 67(3): 345-366.

Figuerola, E.L.M., Guerrero, L.D., Rosa, S.M., Simonetti, L., Duval, M.E., Galantini, J.A., Bedano, J.C., Wall, L.G. and Erijman, L. 2012. Bacterial indicator of agricultural management for soil under no-till crop production. PLoS ONE 7(11): e51075.

Fitria, A.D., and Kurniawan, S. 2021. Land-use changes and slope positions impact on the degradation of soil functions in nutrient stock within the Kalikungkuk micro watershed, East Java, Indonesia. Journal of Degraded and Mining Lands Management 8(2): 2689–2702.

Flores-Rentería, D., Rincón, A., Valladares, F. and Curiel Yuste, J. 2016. Agricultural matrix affects differently the alpha and beta structural and functional diversity of soil microbial communities in a fragmented Mediterranean holm oak forest. Soil Biology and Biochemistry 92: 79-90.

Flores-Rentería, D., Sánchez-Gallén, I., Morales-Rojas, D., Larsen, J. and Ãlvarez-Sánchez, J. 2020. Changes in the abundance and composition of a microbial community associated with land use change in a Mexican tropical rain forest. Journal of Soil Science and Plant Nutrition 20(3): 1144-1155.

Garbisu, C., Alkorta, I. and Epelde, L. 2011. Assessment of soil quality using microbial properties and attributes of ecological relevance. Applied Soil Ecology 49(1): 1-4.

Guo, X., Chen, H.Y.H., Meng, M., Biswas, S.R., Ye, L. and Zhang, J. 2016. Effects of land use change on the composition of soil microbial communities in a managed subtropical forest. Forest Ecology and Management 373: 93-99.

Haichar, F.el Z., Santaella, C., Heulin, T. and Achouak, W. 2014. Root exudates mediated interactions belowground. Soil Biology and Biochemistry 77: 69-80.

Hamady, M., Lozupone, C. and Knight, R. 2010. Fast UniFrac: Facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME Journal 4(1): 17-27.

Hendershot, J.N., Read, Q.D., Henning, J.A., Sanders, N.J. and Classen, A.T. 2017. Consistently inconsistent drivers of microbial diversity and abundance at macroecological scales. Ecology 98(7): 1757-1763.

Hermans, S.M., Buckley, H.L., Case, B.S., Curran-Cournane, F., Taylor, M. and Lear, G. 2017. Bacteria as emerging indicators of soil condition. Applied and Environmental Microbiology 83(1): 1-13.

Hess, M., Sczyrba, A., Egan, R., Kim, T.W., Chokhawala, H., Schroth, G., Luo, S., Clark, D.S., Chen, F., Zhang, T., Mackie, R.I., Pennacchio, L.A., Tringe, S.G., Visel, A., Woyke, T., Wang, Z. and Rubin, E.M. 2011. Metagenomic discovery of biomass-degrading genes and genomes from cow rumen. Science 331(6016): 463-467.

Huang, J., Hu, B., Qi, K., Chen, W., Pang, X., Bao, W. and Tian, G. 2016. Effects of phosphorus addition on soil microbial biomass and community composition in a subalpine spruce plantation. European Journal of Soil Biology 72: 35-41.

Jangid, K., Williams, M.A., Franzluebbers, A.J., Schmidt, T.M., Coleman, D.C. and Whitman, W.B. 2011. Land-use history has a stronger impact on soil microbial community composition than aboveground vegetation and soil properties. Soil Biology and Biochemistry 43(10): 2184-2193.

Jesus, E.D.C., Marsh, T.L., Tiedje, J.M. and Moreira, F.M.D. S. 2009. Changes in land use alter the structure of bacterial communities in Western Amazon soils. ISME Journal 3(9): 1004-1011.

Jiménez-Bueno, N.G., Valenzuela-Encinas, C., Marsch, R., Ortiz-Gutiérrez, D., Verhulst, N., Govaerts, B., Dendooven, L. and Navarro-Noya, Y.E. 2016. Bacterial indicator taxa in soils under different long-term agricultural management. Journal of Applied Microbiology 120(4): 921-933.

Jones, R.T., Robeson, M.S., Lauber, C.L., Hamady, M., Knight, R. and Fierer, N. 2009. A comprehensive survey of soil Acidobacterial diversity using pyrosequencing and clone library analyses. ISME Journal 3(4): 442-453.

Kopecky, J., Kyselkova, M., Omelka, M., Cermak, L., Novotna, J., Grundmann, G.L., Moënne-Loccoz, Y. and Sagova-Mareckova, M. 2011. Actinobacterial community dominated by a distinct clade in acidic soil of a waterlogged deciduous forest. FEMS Microbiology Ecology 78(2): 386-394.

Kumar, M., Brader, G., Sessitsch, A., Mäki, A., van Elsas, J.D., and Nissinen, R. 2017. Plants assemble species specific bacterial communities from common core taxa in three arcto-alpine climate zones. Frontiers in Microbiology 8: 12.

Lee, S.A., Kim, J.M., Kim, Y., Joa, J.H., Kang, S.S., Ahn, J.H., Kim, M., Song, J. and Weon, H.Y. 2020. Different types of agricultural land use drive distinct soil bacterial communities. Scientific Reports 10(17418):1-12.

Lee-Cruz, L., Edwards, D.P., Tripathi, B.M. and Adams, J.M. 2013. Impact of logging and forest conversion to oil palm plantations on soil bacterial communities in Borneo. Applied and Environmental Microbiology 79(23): 7290-7297.

Li, C., Fultz, L.M., Moore-Kucera, J., Acosta-Martínez, V., Kakarla, M. and Weindorf, D.C. 2018. Soil microbial community restoration in Conservation Reserve Program semi-arid grasslands. Soil Biology and Biochemistry 118: 166-177.

Liu, J., Jia, X., Yan, W., Zhong, Y. and Shangguan, Z. 2020. Changes in soil microbial community structure during long-term secondary succession. Land Degradation & Development 31(9): 1151-1166.

Lozupone, C.A., Hamady, M., Kelley, S.T. and Knight, R. 2007. Quantitative and qualitative diversity measures lead to different insights into factors that structure microbial communities. Applied And Environmental Microbiology 73(5): 1576-1585.

Lozupone, C. and Knight, R. 2005. UniFrac: A new phylogenetic method for comparing microbial communities. Applied and Environmental Microbiology 71(12): 8228-8235.

Lozupone, C., Hamady, M. and Knight, R. 2006. UniFrac - An online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics 7(1): 371.

Lozupone, C., Lladser, M.E., Knights, D., Stombaugh, J. and Knight, R. 2011. UniFrac: An effective distance metric for microbial community comparison. ISME Journal 5(2): 169-172.

Mander, C., Wakelin, S., Young, S., Condron, L. and O'Callaghan, M. 2012. Incidence and diversity of phosphate-solubilising bacteria are linked to phosphorus status in grassland soils. Soil Biology and Biochemistry 44(1): 93-101.

Meng, M., Lin, J., Guo, X., Liu, X., Wu, J., Zhao, Y. and Zhang, J. 2019. Impacts of forest conversion on soil bacterial community composition and diversity in subtropical forests. Catena 175: 167-173.

Miyashita, N.T., Iwanaga, H., Charles, S., Diway, B., Sabang, J. and Chong, L. 2013. Soil bacterial community structure in five tropical forests in Malaysia and one temperate forest in Japan revealed by pyrosequencing analyses of 16S rRNA gene sequence variation. Genes and Genetic Systems 88(2): 93-103.

Preem, J.K., Truu, J., Truu, M., Mander, Ü., Oopkaup, K., Lõhmus, K., Helmisaari, H.S., Uri, V. and Zobel, M. 2012. Bacterial community structure and its relationship to soil physico-chemical characteristics in alder stands with different management histories. Ecological Engineering 49: 10-17.

Prescott, C.E., and Grayston, S.J. 2013. Tree species influence on microbial communities in litter and soil: Current knowledge and research needs. Forest Ecology and Management 309: 19-27.

Rodrigues, J.L.M., Pellizari, V.H., Mueller, R., Baek, K., Jesus, E.D.C., Paula, F.S., Mirza, B., Hamaou, G.S., Tsai, S.M., Feiglf, B., Tiedje, J.M., Bohannan, B.J.M. and Nusslein, K. 2013. Conversion of the Amazon rainforest to agriculture results in biotic homogenisation of soil bacterial communities. Proceedings of the National Academy of Sciences of the United States of America 110(3): 988-993.

Sengupta, A., Hariharan, J., Grewal, P.S. and Dick, W.A. 2020. Bacterial community dissimilarity in soils is driven by long-term land-use practices. Agrosystems, Geosciences & Environment 3(1): 1-13.

Suleiman, A.K.A., Manoeli, L., Boldo, J.T., Pereira, M.G. and Roesch, L.F.W. 2013. Shifts in soil bacterial community after eight years of land-use change. Systematic and Applied Microbiology 36(2): 137-144.

Sun, Y., Luo, C., Jiang, L., Song, M., Zhang, D., Li, J., Li, Y., Ostle, N.J. and Zhang, G. 2020. Land-use changes alter soil bacterial composition and diversity in tropical forest soil in China. Science of the Total Environment 712: 136526.

Tripathi, B.M., Kim, M., Singh, D., Lee-Cruz, L., Lai-Hoe, A., Ainuddin, A.N., Go, R., Rahim, R.A., Husni, M.H.A., Chun, J. and Adams, J.M. 2012. Tropical soil bacterial communities in Malaysia: pH dominates in the equatorial tropics too. Microbial Ecology 64(2): 474-484.

Tripathi, B.M., Moroenyane, I. and Adams, J.M. 2017. The impact of agriculture on soil microbial community composition and diversity in Southeast Asia. In Microbes for Climate Resilient Agriculture (pp. 25-40). John Wiley & Sons, Inc.

Trivedi, P., Delgado-Baquerizo, M., Anderson, I.C. and Singh, B.K. 2016. Response of soil properties and microbial communities to agriculture: Implications for primary productivity and soil health indicators. Frontiers in Plant Science 7: 990.

Verhulst, N., Govaerts, B., Verachtert, E., Castellanos-Navarrete, A., Mezzalama, M., Wall, P.C., Chocobar, A., Deckers, J. and Sayre, K.D. 2010. Conservation agriculture, improving soil quality for sustainable production systems? In Food Security and Soil Quality (pp. 137-208). CRC Press.

Vitali, F., Mastromei, G., Senatore, G., Caroppo, C. and Casalone, E. 2016. Long lasting effects of the conversion from natural forest to poplar plantation on soil microbial communities. Microbiological Research 182: 89-98.

Wilcove, D.S., Giam, X., Edwards, D.P., Fisher, B. and Koh, L.P. 2013. Navjot's nightmare revisited: Logging, agriculture, and biodiversity in Southeast Asia. Trends in Ecology and Evolution 28(9): 531-540).

Wu, S.-J., Deng, J.-J., Yin, Y., Qin, S.-J., Zhu, W.-X., Zhou, Y.-B., Wang, B., Ruan, H. and Jin, L. 2019. Bacterial community changes associated with land use type in the forest montane region of Northeast China. Forests 11(1): 40.

Yao, M., Rui, J., Niu, H., Heděnec, P., Li, J., He, Z., Wang, J., Cao, W. and Li, X. 2017. The differentiation of soil bacterial communities along a precipitation and temperature gradient in the eastern Inner Mongolia steppe. Catena 152: 47-56.

Youssef, N., Sheik, C.S., Krumholz, L.R., Najar, F.Z., Roe, B.A. and Elshahed, M.S. 2009. Comparison of species richness estimates obtained using nearly complete fragments and simulated pyrosequencing-generated fragments in 16S rRNA gene-based environmental surveys. Applied and Environmental Microbiology 75(16): 5227-5236.

Yusuf, M., Fernandes, A.A.R., Kurniawan, S. and Arisoesilaningsih, E. 2020. Initial soil properties of the restored degraded area under different vegetation cover in UB Forest, East Java, Indonesia. Journal of Physics: Conference Series 1563(1): 012006.

Zhang, B., Wu, X., Tai, X., Sun, L., Wu, M., Zhang, W., Chen, X., Zhang, G., Chen, T., Liu, G. and Dyson, P. 2019. Variation in Actinobacterial community composition and potential function in different soil ecosystems belonging to the arid Heihe river basin of Northwest China. Frontiers in Microbiology 10: 2209.

Zhang, C., Liu, G., Xue, S. and Wang, G. 2016. Soil bacterial community dynamics reflect changes in plant community and soil properties during the secondary succession of abandoned farmland in the Loess Plateau. Soil Biology and Biochemistry 97: 40-49.

Zhao, Q., Xiong, W., Xing, Y., Sun, Y., Lin, X. and Dong, Y. 2018. Long-term coffee monoculture alters soil chemical properties and microbial communities. Scientific Reports 8(1): 1–11.

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Submitted

24-03-2021

Accepted

28-04-2021

Published

01-07-2021

How to Cite

Yusuf, M., Fernandes, A. A. R., Kurniawan, S., & Arisoesilaningsih, E. (2021). Spatial variation of soil bacteria communities and its alpha diversity as a potential bioindicator of land degradation. Journal of Degraded and Mining Lands Management, 8(4), 2847–2860. https://doi.org/10.15243/jdmlm.2021.084.2847

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Research Article

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