Comparative metagenomic analysis of bacterial diversity in three distantly related soils in India
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Abstract
Soil microbial diversity is a vital factor for the progression of vegetation and biogeochemical cycles in an ecosystem. It is affected by the chemical composition, soil microenvironment and anthropogenic activities. The present study investigated the effect of environmental conditions and anthropogenic activities on the bacterial diversity of three distantly related soils in India. The multiple soil samples were collected from Hospital waste sites (BTC2) with extensive anthropogenic activity, Himalayan forest soil (RM1) with low anthropogenic activity and Tso Kar Lake sediment soil samples with negligible anthropogenic activity with environmental factors such as soil pH, temperature and altitude on the bacterial diversity. The soil samples were analyzed for physico-chemical properties that suggest significant variations in pH, electrical conductivity (EC), total dissolved solids (TDS), temperature and altitude. The SEM-EDS (Scanning electron microscopy with energy-dispersive X-ray spectroscopy) analysis revealed the elemental composition of the soil samples. The bacterial diversity of three different soil samples was studied using 16S rRNA sequencing-based metagenomic analysis. The results suggested that the bacterial diversity in Hospital waste site soil samples was higher than in the other two soil samples based on chao1 (richness and evenness) analysis. The Phyla Firmicutes were more abundant in Hospital waste site soil, and Himalayan forest soil showed a higher abundance of phylum Proteobacteria (28.86%) and Actinobacteria (26.70%). Tso Kar Lake sediment soil samples showed the most abundant phylum as Proteobacteria (46.28%). The study suggests that increased anthropogenic activity increases soil bacterial diversity. It may eventually help to develop new approaches for sustainable land-use management practices.
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Keywords
Anthropogenic activity, Bacterial diversity, Himalayan forest, Metagenomics, Tso Kar Lake
References
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Badger, M.R. & Bek, E.J. (2008). Multiple Rubisco forms in proteobacteria: their functional signifcance in relation to CO2 acquisition by the CBB cycle. J. Exp. Bot. 59:1525–1541. https://doi: 10.1093/jxb/erm297. Epub 2008 Feb 2.
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Bik, E.M., Eckburg, P.B., Gill, S.R., Nelson, KE. & Purdom, E.A. (2006). Molecular analysis of the bacterial microbiota in the human stomach. Proc. Natl. Acad. Sci. USA 103:732–737.
Capolongo, S., Gola, M., di Noia, M., Nickolova, M., Nachiero, D., Rebecchi, A., et al. (2016). Social sustainability in healthcare facilities: a rating tool for analyzing and improving social aspects in environments of care. Ann. Ist Super Sanità., 52(1):15–23. https:// doi:10.4415/ANN_16_01_06.
Chodak, M., Gołe biewski, M., Morawska Płoskonka, J., Kuduk, K. & Niklin ́ska, M. (2013). Diversity of microorganisms from forest soils differently polluted with heavy metals. Appl. Soil. Ecol. 64, 7–14. https://doi.org/10.1016/j.apsoil.2012.11.004.
Douglas, G.M., Maffei, V.J., Zaneveld, J.R., Yurgel, S.N., Brown, J.R., Taylor, C.M., Huttenhower, C. & Langille, M. (2020). PICRUSt2 for prediction of metagenome functions. Nat. Biotechnol., 38:685–688.
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Huet, S., Romdhane, S., Breuil, M. C., Bru, D., Mounier, A., Spor, A., et al. (2023). Experimental community coalescence sheds light on microbial interactions in soil and restores impaired functions. Microbiome 11:7. doi: 10.1186/s40168-023-01480-7.
Handelsman, J. (2004). Metagenomics: application of genomics to uncultured microorganisms. Microbiol Mol Biol Rev., 68(4):669-85. doi: 10.1128/MMBR.68.4.669-685.2004. PMID: 15590779; PMCID: PMC539003.
Ingham, E.R. (2009). Soil biology primer, Chapter 4: Soil fungus. Soil and Water Conservation 22–23 (Soil and Water Conservation Society, 2009).
Jackson, M. (1973). Soil chemical analysis. Prentice-Hall of India Private Limited, New Delhi, India, pp 498.
Joshi, D., Kumar, S., Suyal, DC. & Goel R. (2017). The Microbiome of the Himalayan Ecosystem. Springer Nature Singapore Pte Ltd., 2017 101 V.C. Kalia et al. (eds.), Mining of Microbial Wealth and Meta Genomics, https://doi 10.1007/978-981-10-5708-3_6.
Khan, A.A., Pant, N.C., Sarkar, A., Tandon, S.K., Thamban, M. & Mahalinganathan, K. (2017). The Himalayan cryosphere: A critical assessment and evaluation of glacial melt fraction in the Bhagirathi basin. Geo Front. 8:107–115. https://doi: 10.1016j.gsf.2015.12.009.
Kersters, K., De Vos, P., Gillis, M., Swings, J., Vandamme, P. & Stackebrandt, E. (2006). Introduction to the Proteobacteria. In M Dworkin, S., Falkow, E., Rosenberg, K.H., Schleifer, & E, Stackebrandt. (Eds.), The Prokaryotes : a handbook on the biology of bacteria: Vol. 5 :Proteobacteria : alpha and beta subclasses (3rd ed., pp. 3–37). https://doi.org/10.1007/0-387-30745-1_1.
King, P., Pham, L.K., Waltz, S., Sphar, D., Yamamoto, R.T., Conrad, D., Taplitz, R., Torriani, F. & Forsyth, R.A. (2016). Longitudinal metagenomic analysis of hospital air identifies clinically relevant microbes. PloS one 11(8), e0160124. https://doi.org/10.1371/journal.pone.0160124.
Manish & Pandit (2018). Geophysical upheavals and evolutionary diversification of plant species in the Hi- malaya. PeerJ 6:e5919; https://DOI 10.7717/peerj.5919
Mishra, R.K., Mohammad, N. & Roychoudhury, N. (2016). Soil pollution: Causes, effects and control. Tropical Forest Research Institute, Jabalpur, MP, India. 3 (1).
Ndao, A. & Adjallé, K. (2023). Overview of the Biotransformation of Limonene and α-Pinene from Wood and Citrus Residues by Microorganisms. Waste 2023., 1, 841-859. https://doi.org/10.3390/waste1040049.
Olanrewaju, O.S. & Babalola, O.O., (2019) Streptomyces: implications and interactions in plant growth promotion. Appl. Microbiol. Biotechnol. 103(3):1179-1188. https://doi: 10.1007/s00253-018-09577-y. Epub 2018 Dec 29. PMID: 30594952; PMCID: PMC6394478.
Philip, S. & Singh, N. (2020). Comparative soil analysis by Scanning Electron Microscope: A forensic perspective. Int. J. Emerg. Technol. 11(2): 915-923.
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J. & Gloeckner, F.O. (2013). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res., 41(D1):590–596. https://doi: 10.1093/nar/gks1219. Epub 2012 Nov 28.
Roesch, L. F. W. et al. (2007). Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J. 1(4), 283–290. https://doi.org/ 10.1038/ismej.2007.53.
Rathour, R., Gupta, J., Kumar, M., Hiloidhari, M., Mehrotra, A.K. & Thakur, I.S. (2017). Metagenomic sequencing of microbial communities from brackish water of Pangong Lake of the Northwest Indian Himalayas. Genome announc 5(40), e01029-17. https://doi.org/10.1128/genomeA.01029-17.
Ren, C., Zhang, W., Zhong, Z., Han, X., Yang, G., Feng, Y. & Ren, G. (2018). Differential responses of soil microbial biomass, diversity, and compositions to altitudinal gradients depend on plant and soil characteristics. Sci. Total Environ. 610–611:750–8. https://doi.org/10.1016/j.scitotenv.2017.08.110.
Sankhwar, R., Kumar, A., Yadav, S., Singh, V. & Gupta, RK .(2023). Emycin-E purified from Streptomyces sp. RG1011 from Himalayan soil has antibiofilm activity against Staphylococcus aureus. Microb. Pathog., 182, 106256. https://doi.org/10.1016/j.micpath.2023.10 6256.
Shen, C., Ni. Y., Liang, W., Wang, J. & Chu H. (2015). Distinct soil bacterial communities along a small-scale elevational gradient in alpine tundra. Front. Microbiol., 6:582. https://doi.org/10.3389/fmicb.2015.00582 PMID: 26217308.
Spain, A. M., Krumholz, L. R., & Elshahed, M. S. (2009). Composition, diversity and novelty of soil Proteobacteria. Int. Soc. Microb. Ecol. J., 3 (8):992-1000. https://doi: 10.1038/ismej.2009.43. Epub 2009 Apr 30.
Sharma, N., Kumar, J., Abedin, MM., Sahoo, D., Pandey, A., Rai, A.K. & Singh ,S.P. (2020). Metagenomics revealing molecular profiling of community structure and metabolic pathways in natural hot springs of the Sikkim Himalaya. BMC Microbial., 20(1), 246. https://doi.org/10.1186/s12866-020-01923-3.
Spalding, M.D & Prigge, S.T. (2010). Lipoic acid metabolism in microbial pathogens. Microbiol. Mol. Biol. Rev.74(2):200-28. https://doi: 10.1128/MMBR.00008-10. PMID: 20508247; PMCID: PMC2884412.
Savithiry, N., Gage, D., Fu W et al. (1998). Degradation of Pinene by Bacillus pallidus BR425. Biodegradation 9., 337–341. https://doi.org/10.1023/A:1008304603734.
Singh,S., Chaudhary D. & Verma, S.K. ( 2023). Soil Microorganism and their Role. Volume-2, Issue-3, January, 2023. E-ISSN: 2583-1755.
Sharma, S., Kaur, S. (2021). Soil Microbial Diversity & Metagenomics. In: Cruz, C., Vishwakarma, K., Choudhary, D.K., Varma, A. (eds) Soil Nitrogen Ecology. Soil Biology, vol 62. Springer, Cham. https://doi.org/10.1007/978-3-030-71206-8_14.
Xie, M., An, F., Zhao, Y., Wu, R. & Wu, J. (2020). Metagenomic analysis of bacterial community structure and functions during the fermentation of da-jiang, a Chinese traditional fermented food, LWT. 129, 109450, ISSN 0023-6438, https://doi.org/10.1016/j.lwt.2020.109450.
Wang, Y., Sheng, H.F., He, Y., Wu, J.Y., Jiang, Y.X., Tam, N.F. & Zhou, H.W. (2012). Comparison of the levels of bacterial diversity in freshwater, intertidal wetland, and marine sediments by using millions of illumina tags. Appl. Environ. Microbiol. 78(23), 8264–8271. https://doi.org/10.1128/AEM.01821-12.
Boyce, J.M., Potter-Bynoe, G., Chenevert, C. & King T. (1997). Environmental contamination due to methicillin-resistant Staphylococcus aureus: possible infection control implications. Infect. Control Hosp. Epidemiol. 18(9), 622–627.
Badger, M.R. & Bek, E.J. (2008). Multiple Rubisco forms in proteobacteria: their functional signifcance in relation to CO2 acquisition by the CBB cycle. J. Exp. Bot. 59:1525–1541. https://doi: 10.1093/jxb/erm297. Epub 2008 Feb 2.
Bishop, B.C. & Chatterjee Shiba, P. (2023). "Himalayas". Encyclopedia Britannica, 19 Dec. 2023, https://www.britannica.com/place/Himalayas. Accessed 21 December 2023.
Bik, E.M., Eckburg, P.B., Gill, S.R., Nelson, KE. & Purdom, E.A. (2006). Molecular analysis of the bacterial microbiota in the human stomach. Proc. Natl. Acad. Sci. USA 103:732–737.
Capolongo, S., Gola, M., di Noia, M., Nickolova, M., Nachiero, D., Rebecchi, A., et al. (2016). Social sustainability in healthcare facilities: a rating tool for analyzing and improving social aspects in environments of care. Ann. Ist Super Sanità., 52(1):15–23. https:// doi:10.4415/ANN_16_01_06.
Chodak, M., Gołe biewski, M., Morawska Płoskonka, J., Kuduk, K. & Niklin ́ska, M. (2013). Diversity of microorganisms from forest soils differently polluted with heavy metals. Appl. Soil. Ecol. 64, 7–14. https://doi.org/10.1016/j.apsoil.2012.11.004.
Douglas, G.M., Maffei, V.J., Zaneveld, J.R., Yurgel, S.N., Brown, J.R., Taylor, C.M., Huttenhower, C. & Langille, M. (2020). PICRUSt2 for prediction of metagenome functions. Nat. Biotechnol., 38:685–688.
D’Alessandro, D., Tedesco, P., Rebecchi, A. & Capolongo, S .(2016). Water use and water saving in Italian hospitals. A preliminary investigation. Ann Ist Super Sanita., 52(1):56–62. https://doi:10.4415/ ANN_16_01_11.
Huet, S., Romdhane, S., Breuil, M. C., Bru, D., Mounier, A., Spor, A., et al. (2023). Experimental community coalescence sheds light on microbial interactions in soil and restores impaired functions. Microbiome 11:7. doi: 10.1186/s40168-023-01480-7.
Handelsman, J. (2004). Metagenomics: application of genomics to uncultured microorganisms. Microbiol Mol Biol Rev., 68(4):669-85. doi: 10.1128/MMBR.68.4.669-685.2004. PMID: 15590779; PMCID: PMC539003.
Ingham, E.R. (2009). Soil biology primer, Chapter 4: Soil fungus. Soil and Water Conservation 22–23 (Soil and Water Conservation Society, 2009).
Jackson, M. (1973). Soil chemical analysis. Prentice-Hall of India Private Limited, New Delhi, India, pp 498.
Joshi, D., Kumar, S., Suyal, DC. & Goel R. (2017). The Microbiome of the Himalayan Ecosystem. Springer Nature Singapore Pte Ltd., 2017 101 V.C. Kalia et al. (eds.), Mining of Microbial Wealth and Meta Genomics, https://doi 10.1007/978-981-10-5708-3_6.
Khan, A.A., Pant, N.C., Sarkar, A., Tandon, S.K., Thamban, M. & Mahalinganathan, K. (2017). The Himalayan cryosphere: A critical assessment and evaluation of glacial melt fraction in the Bhagirathi basin. Geo Front. 8:107–115. https://doi: 10.1016j.gsf.2015.12.009.
Kersters, K., De Vos, P., Gillis, M., Swings, J., Vandamme, P. & Stackebrandt, E. (2006). Introduction to the Proteobacteria. In M Dworkin, S., Falkow, E., Rosenberg, K.H., Schleifer, & E, Stackebrandt. (Eds.), The Prokaryotes : a handbook on the biology of bacteria: Vol. 5 :Proteobacteria : alpha and beta subclasses (3rd ed., pp. 3–37). https://doi.org/10.1007/0-387-30745-1_1.
King, P., Pham, L.K., Waltz, S., Sphar, D., Yamamoto, R.T., Conrad, D., Taplitz, R., Torriani, F. & Forsyth, R.A. (2016). Longitudinal metagenomic analysis of hospital air identifies clinically relevant microbes. PloS one 11(8), e0160124. https://doi.org/10.1371/journal.pone.0160124.
Manish & Pandit (2018). Geophysical upheavals and evolutionary diversification of plant species in the Hi- malaya. PeerJ 6:e5919; https://DOI 10.7717/peerj.5919
Mishra, R.K., Mohammad, N. & Roychoudhury, N. (2016). Soil pollution: Causes, effects and control. Tropical Forest Research Institute, Jabalpur, MP, India. 3 (1).
Ndao, A. & Adjallé, K. (2023). Overview of the Biotransformation of Limonene and α-Pinene from Wood and Citrus Residues by Microorganisms. Waste 2023., 1, 841-859. https://doi.org/10.3390/waste1040049.
Olanrewaju, O.S. & Babalola, O.O., (2019) Streptomyces: implications and interactions in plant growth promotion. Appl. Microbiol. Biotechnol. 103(3):1179-1188. https://doi: 10.1007/s00253-018-09577-y. Epub 2018 Dec 29. PMID: 30594952; PMCID: PMC6394478.
Philip, S. & Singh, N. (2020). Comparative soil analysis by Scanning Electron Microscope: A forensic perspective. Int. J. Emerg. Technol. 11(2): 915-923.
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J. & Gloeckner, F.O. (2013). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res., 41(D1):590–596. https://doi: 10.1093/nar/gks1219. Epub 2012 Nov 28.
Roesch, L. F. W. et al. (2007). Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J. 1(4), 283–290. https://doi.org/ 10.1038/ismej.2007.53.
Rathour, R., Gupta, J., Kumar, M., Hiloidhari, M., Mehrotra, A.K. & Thakur, I.S. (2017). Metagenomic sequencing of microbial communities from brackish water of Pangong Lake of the Northwest Indian Himalayas. Genome announc 5(40), e01029-17. https://doi.org/10.1128/genomeA.01029-17.
Ren, C., Zhang, W., Zhong, Z., Han, X., Yang, G., Feng, Y. & Ren, G. (2018). Differential responses of soil microbial biomass, diversity, and compositions to altitudinal gradients depend on plant and soil characteristics. Sci. Total Environ. 610–611:750–8. https://doi.org/10.1016/j.scitotenv.2017.08.110.
Sankhwar, R., Kumar, A., Yadav, S., Singh, V. & Gupta, RK .(2023). Emycin-E purified from Streptomyces sp. RG1011 from Himalayan soil has antibiofilm activity against Staphylococcus aureus. Microb. Pathog., 182, 106256. https://doi.org/10.1016/j.micpath.2023.10 6256.
Shen, C., Ni. Y., Liang, W., Wang, J. & Chu H. (2015). Distinct soil bacterial communities along a small-scale elevational gradient in alpine tundra. Front. Microbiol., 6:582. https://doi.org/10.3389/fmicb.2015.00582 PMID: 26217308.
Spain, A. M., Krumholz, L. R., & Elshahed, M. S. (2009). Composition, diversity and novelty of soil Proteobacteria. Int. Soc. Microb. Ecol. J., 3 (8):992-1000. https://doi: 10.1038/ismej.2009.43. Epub 2009 Apr 30.
Sharma, N., Kumar, J., Abedin, MM., Sahoo, D., Pandey, A., Rai, A.K. & Singh ,S.P. (2020). Metagenomics revealing molecular profiling of community structure and metabolic pathways in natural hot springs of the Sikkim Himalaya. BMC Microbial., 20(1), 246. https://doi.org/10.1186/s12866-020-01923-3.
Spalding, M.D & Prigge, S.T. (2010). Lipoic acid metabolism in microbial pathogens. Microbiol. Mol. Biol. Rev.74(2):200-28. https://doi: 10.1128/MMBR.00008-10. PMID: 20508247; PMCID: PMC2884412.
Savithiry, N., Gage, D., Fu W et al. (1998). Degradation of Pinene by Bacillus pallidus BR425. Biodegradation 9., 337–341. https://doi.org/10.1023/A:1008304603734.
Singh,S., Chaudhary D. & Verma, S.K. ( 2023). Soil Microorganism and their Role. Volume-2, Issue-3, January, 2023. E-ISSN: 2583-1755.
Sharma, S., Kaur, S. (2021). Soil Microbial Diversity & Metagenomics. In: Cruz, C., Vishwakarma, K., Choudhary, D.K., Varma, A. (eds) Soil Nitrogen Ecology. Soil Biology, vol 62. Springer, Cham. https://doi.org/10.1007/978-3-030-71206-8_14.
Xie, M., An, F., Zhao, Y., Wu, R. & Wu, J. (2020). Metagenomic analysis of bacterial community structure and functions during the fermentation of da-jiang, a Chinese traditional fermented food, LWT. 129, 109450, ISSN 0023-6438, https://doi.org/10.1016/j.lwt.2020.109450.
Wang, Y., Sheng, H.F., He, Y., Wu, J.Y., Jiang, Y.X., Tam, N.F. & Zhou, H.W. (2012). Comparison of the levels of bacterial diversity in freshwater, intertidal wetland, and marine sediments by using millions of illumina tags. Appl. Environ. Microbiol. 78(23), 8264–8271. https://doi.org/10.1128/AEM.01821-12.
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Comparative metagenomic analysis of bacterial diversity in three distantly related soils in India. (2024). Journal of Applied and Natural Science, 16(3), 987-997. https://doi.org/10.31018/jans.v16i3.5635
