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References

  1. Cowan DA, Makhalanyane TP, Dennis PG, Hopkins DW. 2014. Microbial ecology and biogeochemistry of continental Antarctic soils. Front. Microbiol. 5: 154.
    Pubmed PMC CrossRef
  2. Makhalanyane TP, Valverde A, Gunnigle E, Frossard A, Ramond JB, Cowan DA. 2015. Microbial ecology of hot desert edaphic systems. FEMS Microbiol. Rev. 39: 203-221.
    Pubmed CrossRef
  3. Jones FT, Wineland MJ, Parsons JT, Hagler WM. 1996. Degradation of aflatoxin by poultry litter. Poult. Sci. 75: 52-58.
    Pubmed CrossRef
  4. Elbert T, Pantev C, Wienbruch C, Rockstroh B, Taub E. 1995. Increased cortical representation of the fingers of the left hand in string players. Science 270: 305-307.
    Pubmed CrossRef
  5. Belap J, Welter JR, Grimm, NB, Barger N, Ludwig JA. 2005. Linkages between microbial and hydrologic processes in arid and semiarid watersheds. Ecology 86: 298-307.
    CrossRef
  6. Housman DC, Yeager CM, Darby BJ, Sanford RL, Kuske CR, Neher DA, et al. 2007. Heterogeneity of soil nutrients and subsurface biota in a dryland ecosystem. Soil Biol. Biochem. 39: 2138-2149.
    CrossRef
  7. Geyer KM, Altrichter AE, Van Horn DJ, Takacs-Vesbach CD, Gooseff MN, Barrett JE. 2013. Environmental controls over bacterial communities in polar desert soils. Ecosphere 4: 127.
    CrossRef
  8. Pajares S, Escalante AE, Noguez AM, García-Oliva F, Martínez-Piedragil C, Cram SS, et al. 2016. Spatial heterogeneity of physicochemical properties explains differences in microbial composition in arid soils from CuatroCienegas, Mexico. PeerJ 4: e2459.
    Pubmed PMC CrossRef
  9. Garcia-Pichel F, Loza V, Marusenko Y, Mateo P, Potrafka RM. 2013. Temperature drives the continental-scale distribution of key microbes in topsoil communities. Science 340: 1574-1577.
    Pubmed CrossRef
  10. Ben-David EA, Zaady E, Sher Y, Nejidat A. 2011. Assessment of the spatial distribution of soil microbial communities in patchy arid and semi-arid landscapes of the Negev Desert using combined PLFA and DGGE analyses. FEMS Microbiol. Ecol. 76: 492-503.
    Pubmed CrossRef
  11. Maestre FT, Escudero A, Martínez I, Guerrero C, Rubio A. 2005. Does spatial pattern matter to ecosystem functioning? Insights from biological soil crusts. Funct. Ecol. 19: 566-573.
    CrossRef
  12. Mohammadipanah F, Wink J. 2016.Actinobacteria from arid and desert habitats: diversity and biological activity. Front Microbiol. 6: 1541.
    Pubmed PMC CrossRef
  13. Arocha-Garza HF, Castillo RC-D, Eguiarte LE, Souza V, Torre-Zavala SD. 2017. High diversity and suggested endemicity of culturable Actinobacteria in an extremely oligotrophic desert oasis. PeerJ 5: e3247.
    Pubmed PMC CrossRef
  14. Peel MC, Finlayson BL, McMahonTA. 2007. Updated world map of the Köppen-Geiger climate classification. Hydrol. Earth Syst. Sci. 11: 1633-1644.
    CrossRef
  15. Shyampura RL, Sehgal J. 1995. Soils of Rajasthan for optimizing land use. Soils of India Series, NBSS Pub. 51.
  16. Bower CA, Reitemeier RF, Fireman R. 1972. Exchangeable cations of saline and alkaline soils. Soil Sci. 73: 251-257.
    CrossRef
  17. Walkley A, Black JA. 1934. An estimation of digestion method for determining soil organic matter and a proposed modification of chromic acid titration method. Soil Sci. 37:29-38.
    CrossRef
  18. Jackson ML. 1973. Soil chemical analysis. pp. ??-??. Prentice Hall of India Private Limited, New Delhi.
  19. Keeney DR, Nelson DW. 1982. Nitrogen-inorganic forms, pp. 643-698. In Page AL, Miller RH, Keeney DR (eds.), Methods of soil analysis, Part 2, chemical and microbiological methods. ASA-SSSA, Madison, USA.
  20. Pamberton H. 1945. Estimation of total phosphorus. J Amer. Chem. Soc. 15: 383-395.
  21. Edgar RC. 2013. UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10: 996-998.
    Pubmed CrossRef
  22. Huson DH, Beier S, Flade I, Górska A, El-Hadidi M, Mitra S, et al. 2016. MEGAN community edition-interactive exploration and analysis of large-scale microbiome sequencing data. PLoS Comput. Biol. 12: e1004957.
    Pubmed PMC CrossRef
  23. Colwell RK, Chao A, Gotelli NJ, Lin S-Y, Mao CX, Chazdon RL, et al. 2012. Models and estimators linking individual-based and sample-based rarefaction, extrapolation, and comparison of assemblages. J. Plant Ecol. 5: 3-21.
    CrossRef
  24. Arndt D, Xia J, Liu Y, Zhou Y, Guo AC, Cruz JA, et al. 2012. METAGENassist: A comprehensive web server for comparative metagenomics. Nucleic Acids Res. 40: W88-W95.
    Pubmed PMC CrossRef
  25. Hackstadt AJ, Hess AM. 2009. Filtering for increased power for microarray data analysis. BMC Bioinformatics 10: 11.
    Pubmed PMC CrossRef
  26. Rao S, Chan Y, Bugler-Lacap DC, Bhatnagar A, Bhatnagar M, Stephen B. 2016. Pointing microbial diversity in soil, sand dune and rock substrates of the Thar monsoon desert, India. Indian J. Microbiol. 56: 35-45.
    Pubmed PMC CrossRef
  27. Perry RA, Goodall DW. 2009. Arid Land Ecosystems:structure, functioning and management. Cambridge UK:Cambridge University Press
  28. Yasir M, Azhar EI, Khan I, Bibi F, Baabdullah R, Al-Zahrani IA, et al. 2015. Composition of soil microbiome along elevation gradients in southwestern highlands of Saudi Arabia. BMC Microbiol. 15: 65.
    Pubmed PMC CrossRef
  29. Ronca S, Ramond J-B, Jones BE, Seely M, Cowan DA. 2015. Namib desert dune/interdune transects exhibit habitat-specific edaphic bacterial communities. Front Microbiol. 6: 845.
    Pubmed PMC CrossRef
  30. Wei STS, Lacap-Bugler DC, Lau MCY, Caruso T, Rao S, de los Rios A, et al. 2016. Taxonomic and functional diversity of soil and hypolithic microbial communities in Miers Valley, McMurdo Dry Valleys, Antarctica. Front Microbiol. 7: 1642.
    Pubmed PMC CrossRef
  31. Le PT, Makhalanyane TP, Guerrero LD, Vikram S, Peer YV, Cowan DA. 2016. Comparative metagenomic analysis reveals mechanisms for stress response in hypoliths from extreme hyperarid deserts. Genome Biol. Evol. 8: 2737-2747.
    Pubmed PMC CrossRef
  32. Vikram S, Guerrero LD, Makhalanyane TP, Le PT, Seely M, Cowan DA. 2015. Metagenomic analysis provides insights into functional capacity in a hyperarid desert soil niche community. Environ. Microbiol. 18: 1875-1888.
    Pubmed CrossRef
  33. Barka EA, Vatsa P, Sanchez L, Gaveau-Vaillant N, Jacquard C, Klenk HP, et al. 2016. Taxonomy, physiology, and natural products of Actinobacteria. Microbiol. Mol. Biol. Rev. 80: 1-43.
    CrossRef
  34. Parrot D, Antony-Babu S, Intertaglia L, Grube M, Tomasi S, Suzuki MT. 2015. Littoral lichens as a novel source of potentially bioactive Actinobacteria. Sci. Rep. 5: 15839.
    Pubmed PMC CrossRef
  35. Guo X, Liu N, Li X, Ding Y, Shang F, Gao Y, et al. 2015. Red soils harbour diverse culturable actinomycetes that are promising sources of novel secondary metabolites. Appl. Environ. Microbiol. 81: 3086-3103.
    Pubmed PMC CrossRef
  36. Jose PA, Jha B. 2017. Intertidal marine sediment harbours Actinobacteria with promising bioactive and biosynthetic potential. Sci. Rep. 7: 10041.
    Pubmed PMC CrossRef
  37. Maestre FT, Delgado-Baquerizo M, Jeffries TC, Eldridge DJ, Ochoa V, Gozalo B, et al. 2015. Increasing aridity reduces soil microbial diversity and abundance in global drylands. P. Natl. Acad. Sci. USA 112: 15684-15689.
    CrossRef
  38. Lupatini M, Suleiman AK, Jacques RJ, Antoniolli ZI, Kuramae EE, de Oliveira Camargo FA, et al. 2013. Soil-borne bacterial structure and diversity does not reflect community activity in Pampa biome. PLoS One 8: e76465.
    Pubmed PMC CrossRef
  39. Gorlach-Lira K, Coutinho HDM. 2007. Population dynamics and extracellular enzymes activity of mesophilic and thermophilic bacteria isolated from semi-arid soil of Northeastern Brazil. Braz. J. Microbiol. 38: 135-141.
    CrossRef
  40. Sharma R, Manda R, Gupta S, Kumar S, Kumar V. 2013. Isolation and characterization of osmotolerant bacteria from Thar desert of western Rajasthan (India). Rev. Biol. Trop. 61: 1551-1562.
    Pubmed CrossRef
  41. Bachar A, Soares MIM, Gillor O. 2012. The effect of resource islands on abundance and diversity of bacteria in arid soils. Microbial Ecol. 63: 694-700.
    Pubmed CrossRef
  42. Su LJ, Yang LL, Huang S, Su XQ, Li Y, Wang FQ, et al. 2016. Comparative gut microbiomes of four species representing the higher and the lower termites. J. Insect. Sci. 16: 97.
    Pubmed PMC CrossRef
  43. Llorens-Marès T, Yooseph S, Goll J, Hoffman J, Vila-Costa M, Borrego CM, et al. 2015. Connecting biodiversity and potential functional role in modern euxinic environments by microbial metagenomics. ISME J. 9: 1648-1661.
    Pubmed PMC CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2018; 28(9): 1517-1526

Published online September 28, 2018 https://doi.org/10.4014/jmb.1804.04005

Copyright © The Korean Society for Microbiology and Biotechnology.

Spatial Physiochemical and Metagenomic Analysis of Desert Environment

Kunjukrishnan Kamalakshi Sivakala 1, Polpass Arul Jose 2, Rangasamy Anandham 2, Thangathurai Thinesh 3, S.R.D. Jebakumar 1, Sandipan Samaddar 4, Poulami Chatterjee 4, Natesan Sivakumar 1 and Tongmin Sa 4*

1School of Biotechnology, Madurai Kamaraj University, Madurai, India , 2Department of Agricultural Microbiology, Agricultural College and Research Institute, Tamil Nadu Agricultural University, Madurai, India. , 3School of Life sciences, Pondicherry University, Pudhucherry, India , 4Department of Environmental and Biological Chemistry, Chungbuk National University, Cheongju, Republic of Korea, 5Current affiliation: The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Israel.

Received: April 4, 2018; Accepted: July 11, 2018

Abstract

Investigating the bacterial diversity and their metabolic capabilities are crucial for interpreting ecological patterns in desert environment, and assessing the presence of exploitable microbial resources. In this study, we evaluated the spatial heterogeneity of physico-chemical parameters, soil bacterial diversity and metabolic adaptation at meter scale. Soil samples were collected from two quadrates a desert environment (Thar Desert, India) which face hot arid climate with very little rainfall and extreme temperatures. Analysis of physico-chemical parameters and subsequent variance analysis (p-values < 0.05) revealed that sulfate, potassium and magnesium ions were the most variable between the quadrates. Microbial diversity of the two quadrates was studied using Illumina bar coded sequencing by targeting V3-V4 regions of 16S rDNA. As the results, 702504 high-quality sequence reads, assigned to 173 operationaltaxonomic units (OTUs) at species level. The most abundant phyla in both quadrates were Actinobacteria (38.72%), Proteobacteria (32.94%), and Acidobacteria (9.24%). At genus level, Gaiellarepresented highest prevalence, followed by Streptomyces, Solirubrobacter, Aciditerrimonas, Geminicoccus, Geodermatophilus, Microvirga, and Rubrobacter. Between the quadrates, significant difference (p-values < 0.05) was found in the abundance of Aciditerrimonas, Geodermatophilus Geminicoccus, Ilumatobacter, Marmoricola, Nakamurellaand Solirubrobacter. Metabolic functional mapping revealed diverse biological activities, and was significantly correlated with physico-chemical parameters. The results revealed spatial variation of ions, microbial abundance and functional attributes in the studied quadrates, and patchy nature in local scale. Interestingly, abundance ofthe biotechnologically important phylum Actinobacteria, with large proposition of unclassified speciesin the desert suggested that this arid environment is the promising site for bioprospection.

Keywords: Desert, arid soil, spatial heterogeneity, microbial diversity, functional mapping, Actinobacteria

References

  1. Cowan DA, Makhalanyane TP, Dennis PG, Hopkins DW. 2014. Microbial ecology and biogeochemistry of continental Antarctic soils. Front. Microbiol. 5: 154.
    Pubmed KoreaMed CrossRef
  2. Makhalanyane TP, Valverde A, Gunnigle E, Frossard A, Ramond JB, Cowan DA. 2015. Microbial ecology of hot desert edaphic systems. FEMS Microbiol. Rev. 39: 203-221.
    Pubmed CrossRef
  3. Jones FT, Wineland MJ, Parsons JT, Hagler WM. 1996. Degradation of aflatoxin by poultry litter. Poult. Sci. 75: 52-58.
    Pubmed CrossRef
  4. Elbert T, Pantev C, Wienbruch C, Rockstroh B, Taub E. 1995. Increased cortical representation of the fingers of the left hand in string players. Science 270: 305-307.
    Pubmed CrossRef
  5. Belap J, Welter JR, Grimm, NB, Barger N, Ludwig JA. 2005. Linkages between microbial and hydrologic processes in arid and semiarid watersheds. Ecology 86: 298-307.
    CrossRef
  6. Housman DC, Yeager CM, Darby BJ, Sanford RL, Kuske CR, Neher DA, et al. 2007. Heterogeneity of soil nutrients and subsurface biota in a dryland ecosystem. Soil Biol. Biochem. 39: 2138-2149.
    CrossRef
  7. Geyer KM, Altrichter AE, Van Horn DJ, Takacs-Vesbach CD, Gooseff MN, Barrett JE. 2013. Environmental controls over bacterial communities in polar desert soils. Ecosphere 4: 127.
    CrossRef
  8. Pajares S, Escalante AE, Noguez AM, García-Oliva F, Martínez-Piedragil C, Cram SS, et al. 2016. Spatial heterogeneity of physicochemical properties explains differences in microbial composition in arid soils from CuatroCienegas, Mexico. PeerJ 4: e2459.
    Pubmed KoreaMed CrossRef
  9. Garcia-Pichel F, Loza V, Marusenko Y, Mateo P, Potrafka RM. 2013. Temperature drives the continental-scale distribution of key microbes in topsoil communities. Science 340: 1574-1577.
    Pubmed CrossRef
  10. Ben-David EA, Zaady E, Sher Y, Nejidat A. 2011. Assessment of the spatial distribution of soil microbial communities in patchy arid and semi-arid landscapes of the Negev Desert using combined PLFA and DGGE analyses. FEMS Microbiol. Ecol. 76: 492-503.
    Pubmed CrossRef
  11. Maestre FT, Escudero A, Martínez I, Guerrero C, Rubio A. 2005. Does spatial pattern matter to ecosystem functioning? Insights from biological soil crusts. Funct. Ecol. 19: 566-573.
    CrossRef
  12. Mohammadipanah F, Wink J. 2016.Actinobacteria from arid and desert habitats: diversity and biological activity. Front Microbiol. 6: 1541.
    Pubmed KoreaMed CrossRef
  13. Arocha-Garza HF, Castillo RC-D, Eguiarte LE, Souza V, Torre-Zavala SD. 2017. High diversity and suggested endemicity of culturable Actinobacteria in an extremely oligotrophic desert oasis. PeerJ 5: e3247.
    Pubmed KoreaMed CrossRef
  14. Peel MC, Finlayson BL, McMahonTA. 2007. Updated world map of the Köppen-Geiger climate classification. Hydrol. Earth Syst. Sci. 11: 1633-1644.
    CrossRef
  15. Shyampura RL, Sehgal J. 1995. Soils of Rajasthan for optimizing land use. Soils of India Series, NBSS Pub. 51.
  16. Bower CA, Reitemeier RF, Fireman R. 1972. Exchangeable cations of saline and alkaline soils. Soil Sci. 73: 251-257.
    CrossRef
  17. Walkley A, Black JA. 1934. An estimation of digestion method for determining soil organic matter and a proposed modification of chromic acid titration method. Soil Sci. 37:29-38.
    CrossRef
  18. Jackson ML. 1973. Soil chemical analysis. pp. ??-??. Prentice Hall of India Private Limited, New Delhi.
  19. Keeney DR, Nelson DW. 1982. Nitrogen-inorganic forms, pp. 643-698. In Page AL, Miller RH, Keeney DR (eds.), Methods of soil analysis, Part 2, chemical and microbiological methods. ASA-SSSA, Madison, USA.
  20. Pamberton H. 1945. Estimation of total phosphorus. J Amer. Chem. Soc. 15: 383-395.
  21. Edgar RC. 2013. UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10: 996-998.
    Pubmed CrossRef
  22. Huson DH, Beier S, Flade I, Górska A, El-Hadidi M, Mitra S, et al. 2016. MEGAN community edition-interactive exploration and analysis of large-scale microbiome sequencing data. PLoS Comput. Biol. 12: e1004957.
    Pubmed KoreaMed CrossRef
  23. Colwell RK, Chao A, Gotelli NJ, Lin S-Y, Mao CX, Chazdon RL, et al. 2012. Models and estimators linking individual-based and sample-based rarefaction, extrapolation, and comparison of assemblages. J. Plant Ecol. 5: 3-21.
    CrossRef
  24. Arndt D, Xia J, Liu Y, Zhou Y, Guo AC, Cruz JA, et al. 2012. METAGENassist: A comprehensive web server for comparative metagenomics. Nucleic Acids Res. 40: W88-W95.
    Pubmed KoreaMed CrossRef
  25. Hackstadt AJ, Hess AM. 2009. Filtering for increased power for microarray data analysis. BMC Bioinformatics 10: 11.
    Pubmed KoreaMed CrossRef
  26. Rao S, Chan Y, Bugler-Lacap DC, Bhatnagar A, Bhatnagar M, Stephen B. 2016. Pointing microbial diversity in soil, sand dune and rock substrates of the Thar monsoon desert, India. Indian J. Microbiol. 56: 35-45.
    Pubmed KoreaMed CrossRef
  27. Perry RA, Goodall DW. 2009. Arid Land Ecosystems:structure, functioning and management. Cambridge UK:Cambridge University Press
  28. Yasir M, Azhar EI, Khan I, Bibi F, Baabdullah R, Al-Zahrani IA, et al. 2015. Composition of soil microbiome along elevation gradients in southwestern highlands of Saudi Arabia. BMC Microbiol. 15: 65.
    Pubmed KoreaMed CrossRef
  29. Ronca S, Ramond J-B, Jones BE, Seely M, Cowan DA. 2015. Namib desert dune/interdune transects exhibit habitat-specific edaphic bacterial communities. Front Microbiol. 6: 845.
    Pubmed KoreaMed CrossRef
  30. Wei STS, Lacap-Bugler DC, Lau MCY, Caruso T, Rao S, de los Rios A, et al. 2016. Taxonomic and functional diversity of soil and hypolithic microbial communities in Miers Valley, McMurdo Dry Valleys, Antarctica. Front Microbiol. 7: 1642.
    Pubmed KoreaMed CrossRef
  31. Le PT, Makhalanyane TP, Guerrero LD, Vikram S, Peer YV, Cowan DA. 2016. Comparative metagenomic analysis reveals mechanisms for stress response in hypoliths from extreme hyperarid deserts. Genome Biol. Evol. 8: 2737-2747.
    Pubmed KoreaMed CrossRef
  32. Vikram S, Guerrero LD, Makhalanyane TP, Le PT, Seely M, Cowan DA. 2015. Metagenomic analysis provides insights into functional capacity in a hyperarid desert soil niche community. Environ. Microbiol. 18: 1875-1888.
    Pubmed CrossRef
  33. Barka EA, Vatsa P, Sanchez L, Gaveau-Vaillant N, Jacquard C, Klenk HP, et al. 2016. Taxonomy, physiology, and natural products of Actinobacteria. Microbiol. Mol. Biol. Rev. 80: 1-43.
    CrossRef
  34. Parrot D, Antony-Babu S, Intertaglia L, Grube M, Tomasi S, Suzuki MT. 2015. Littoral lichens as a novel source of potentially bioactive Actinobacteria. Sci. Rep. 5: 15839.
    Pubmed KoreaMed CrossRef
  35. Guo X, Liu N, Li X, Ding Y, Shang F, Gao Y, et al. 2015. Red soils harbour diverse culturable actinomycetes that are promising sources of novel secondary metabolites. Appl. Environ. Microbiol. 81: 3086-3103.
    Pubmed KoreaMed CrossRef
  36. Jose PA, Jha B. 2017. Intertidal marine sediment harbours Actinobacteria with promising bioactive and biosynthetic potential. Sci. Rep. 7: 10041.
    Pubmed KoreaMed CrossRef
  37. Maestre FT, Delgado-Baquerizo M, Jeffries TC, Eldridge DJ, Ochoa V, Gozalo B, et al. 2015. Increasing aridity reduces soil microbial diversity and abundance in global drylands. P. Natl. Acad. Sci. USA 112: 15684-15689.
    CrossRef
  38. Lupatini M, Suleiman AK, Jacques RJ, Antoniolli ZI, Kuramae EE, de Oliveira Camargo FA, et al. 2013. Soil-borne bacterial structure and diversity does not reflect community activity in Pampa biome. PLoS One 8: e76465.
    Pubmed KoreaMed CrossRef
  39. Gorlach-Lira K, Coutinho HDM. 2007. Population dynamics and extracellular enzymes activity of mesophilic and thermophilic bacteria isolated from semi-arid soil of Northeastern Brazil. Braz. J. Microbiol. 38: 135-141.
    CrossRef
  40. Sharma R, Manda R, Gupta S, Kumar S, Kumar V. 2013. Isolation and characterization of osmotolerant bacteria from Thar desert of western Rajasthan (India). Rev. Biol. Trop. 61: 1551-1562.
    Pubmed CrossRef
  41. Bachar A, Soares MIM, Gillor O. 2012. The effect of resource islands on abundance and diversity of bacteria in arid soils. Microbial Ecol. 63: 694-700.
    Pubmed CrossRef
  42. Su LJ, Yang LL, Huang S, Su XQ, Li Y, Wang FQ, et al. 2016. Comparative gut microbiomes of four species representing the higher and the lower termites. J. Insect. Sci. 16: 97.
    Pubmed KoreaMed CrossRef
  43. Llorens-Marès T, Yooseph S, Goll J, Hoffman J, Vila-Costa M, Borrego CM, et al. 2015. Connecting biodiversity and potential functional role in modern euxinic environments by microbial metagenomics. ISME J. 9: 1648-1661.
    Pubmed KoreaMed CrossRef