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Impact of soil salinity on the microbial structure of halophyte rhizosphere microbiome

  • Salma Mukhtar
  • Babur Saeed Mirza
  • Samina Mehnaz
  • Muhammad Sajjad Mirza
  • Joan Mclean
  • Kauser Abdulla MalikEmail author
Original Paper

Abstract

The rhizosphere microbiome plays a significant role in the life of plants in promoting plant survival under adverse conditions. However, limited information is available about microbial diversity in saline environments. In the current study, we compared the composition of the rhizosphere microbiomes of the halophytes Urochloa, Kochia, Salsola, and Atriplex living in moderate and high salinity environments (Khewra salt mines; Pakistan) with that of the non-halophyte Triticum. Soil microbiomes analysis using pyrosequencing of 16S rRNA gene indicated that Actinobacteria were dominant in saline soil samples whereas Proteobacteria predominated in non-saline soil samples. Firmicutes, Acidobacteria, Bacteriodetes and Thaumarchaeota were predominant phyla in saline and non-saline soils, whereas Cyanobacteria, Verrucomicrobia, Gemmatimonadetes and the unclassified WPS-2 were less abundant. Sequences from Euryarchaeota, Ignavibacteriae, and Nanohaloarchaeota were identified only from the rhizosphere of halophytes. Dominant halophilic bacteria and archaea identified in this study included Agrococcus, Armatimonadetes gp4, Halalkalicoccus, Haloferula and Halobacterium. Our analysis showed that increases in soil salinity correlated with significant differences in the alpha and beta diversity of the microbial communities across saline and non-saline soil samples. Having a complete inventory of the soil bacteria from different saline environments in Pakistan will help in the discovery of potential inoculants for crops growing on salt-affected land.

Keywords

Soil microbiome 16S rRNA gene Pyrosequencing Soil salinity Halophilic bacteria Haloarchaea 

Notes

Acknowledgements

We are highly thankful to Higher Education Commission [Project # HEC (FD/2012/1843)] and Pakistan Academy of Sciences [Project # 5-9/PAS/2012/969] for research grants. We would like to express our gratitude to Mr. Mukhtar Ahmad (Assistant Professor), Dyal Singh College, Lahore, for assistance in statistical analyses. We are grateful to Prof. Ann M. Hirsch (UCLA) for the comments on the manuscript.

Author contributions

SM: Conducted experiment and prepared manuscript; BSM: pyrosequencing and data analysis; SM: manuscript preparation; MSM: supervised research and manuscript preparation; JM: pyrosequencing and data analysis; KAM: guided in experiment plan and edited manuscript.

Compliance with ethical standards

Conflict of interest

The authors declared that they have no conflict of interest in the publication.

Supplementary material

11274_2018_2509_MOESM1_ESM.docx (6.9 mb)
Supplementary material 1 (DOCX 7037 KB)

References

  1. Adviento-Borbe MA, Doran JW, Drijber RA, Dobermann A (2006) Soil electrical conductivity and water content affect nitrous oxide and carbon dioxide emissions in intensively managed soils. J Environ Qual 35:1999–2010CrossRefPubMedGoogle Scholar
  2. Ahmad K, Hussain M, Ashraf M, Luqman M, Ashraf MY, Khan ZI (2007) Indigenous vegetation of Soon valley at the risk of extinction. Pak J 39(3):679–690Google Scholar
  3. Ahmad MJ, Arshad M, Iqbal A, Khalid M, Akhtar N (2013) Rice production in salt-affected soils of Pakistan using different reclamation techniques. In: Shahid SA, Abdelfattah MA, Taha FK (eds), Developments in soil salinity assessment and reclamation: innovative thinking and use of marginal soil and water resources in irrigated agriculture Springer, Dordrecht, pp 283–293CrossRefGoogle Scholar
  4. Anderson JM, Ingram JS (1993) Tropical soil biology and fertility: a handbook of methods, 2nd edn. CAB International, Wallingford, pp 93–94Google Scholar
  5. Berendsen RL, Pieterse CMJ, Bakker AHM (2012) The rhizosphere microbiome and plant health. Trends in Plant Sci 17:478–486CrossRefGoogle Scholar
  6. Bodenhausen N, Horton MW, Bergelson J (2013) Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. PLoS ONE 8:e56329CrossRefPubMedPubMedCentralGoogle Scholar
  7. Borcard D, Legendre P, Drapeau P (1992) Partialling out the spatial component of ecological variation. Ecology 14:1045CrossRefGoogle Scholar
  8. Buttigieg PL, Ramette A (2014) A Guide to statistical analysis in microbial ecology: a community-focused, living review of multivariate data analyses. FEMS Microbiol Ecol 90:543–550CrossRefPubMedGoogle Scholar
  9. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K et al (2010) QIIME allows analysis of high throughput community sequencing data. Nat Methods 7:335–336CrossRefPubMedPubMedCentralGoogle Scholar
  10. Chakraborty A, Bera A, Mukherjee A et al (2015) Changing bacterial profile of Sundarbans, the world heritage mangrove: impact of anthropogenic interventions. World J Microbiol Biotechnol 31(4):593–610CrossRefPubMedGoogle Scholar
  11. Craita EB, Tom G (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci 4:1–18Google Scholar
  12. Curlango-rivera G, Huskey DA, Mostafa A, Kessler JO, Xiong Z, Hawes MC (2013) Intraspecies variation in cotton border cell production: rhizosphere microbiome implications. Am J Bot 100:1706–1712CrossRefPubMedGoogle Scholar
  13. Dagla HR, Shekhawat NS (2005) In vitro multiplication of Haloxylon recurvum (Moq.)—a plant for saline soil reclamation. J Plant Biol 7:155–160Google Scholar
  14. Dastgheib SM, Amoozegar MA, Khajeh K, Ventosa A (2011) A halotolerant Alcanivorax sp. strain with potential application in saline soil remediation. Appl Microbiol Biotech 90:305–312CrossRefGoogle Scholar
  15. DeBruyn J, Nixon L, Fawaz M, Johnson M, Radosevich M (2011) Global biogeography and quantitative season dynamics of Gemmatimonadetes in Soil. Appl Environ Microbiol 77(17):6295–6300CrossRefPubMedPubMedCentralGoogle Scholar
  16. Delgado-García M, Aguilar CN, Contreras-Esquivel JC, Rodríguez-Herrera R (2014) Screening for extracellular hydrolytic enzymes production by different halophilic bacteria. Mycopathy 12(1):17–23Google Scholar
  17. Delmont TO, Francioli D, Jacquesson S, Laoudi S, Mathieu A, Nesme J et al (2014) Microbial community development and unseen diversity recovery in inoculated sterile soil. Biol Fert Soil 50:1–8CrossRefGoogle Scholar
  18. Deng S, Chang X, Zhang Y, Ren L, Jiang F, Qu Z, Peng F (2015) Nocardioides antarcticus sp. nov., isolated from marine sediment of Ardley cove. Int J Syst Evol Microbiol 65(8):2615–2621CrossRefPubMedGoogle Scholar
  19. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K et al (2006) Green genes, a chimera checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072CrossRefPubMedPubMedCentralGoogle Scholar
  20. Dodd IC, Perez-Alfocea F (2012) Microbial amelioration of crop salinity stress. J Exp Bot 63(9):3415–3428CrossRefPubMedGoogle Scholar
  21. Doxey AC, Kurtz DA, Lynch MDJ, Sauder LA, Neufeld JD (2015) Aquatic metagenomes implicate Thaumarchaeota in global cobalamin production. ISME J 9:461–471CrossRefPubMedGoogle Scholar
  22. Fahmy T (2003) XLSTAT-Pro 7.0 (XLSTAT). Addinsoft, ParisGoogle Scholar
  23. Fierer N, Leff JW, Adams BJ et al (2012) Cross-biome metagenomic analyses of soilmicrobial communities and their functional attributes. Proc Natl Acad Sci USA 109:21390–21395CrossRefPubMedGoogle Scholar
  24. Garrity GM, Holt JG (2001) Phylum AII. Euryarchaeota phy. nov. In: Boone DR, Castenholz RW (eds) Bergey’s manual of systematic bacteriology volume 1: the archaea and the deeply branching and phototrophic bacteria, 2nd edn. Springer-Verlag, New York, pp 169–192CrossRefGoogle Scholar
  25. Gautier TD (2001) Detecting trends using Spearman’s rank correlation coefficient. Environ Forens 2:359–362CrossRefGoogle Scholar
  26. Ghollarata M, Raiesi F (2007) The adverse effects of soil salinization on the growth of Trifolium alexandrinum L. and associated microbial and biochemical properties in a soil from Iran. Soil Biol Biochem 39:1699–1702CrossRefGoogle Scholar
  27. Ghosh A, Dey N, Bera A, Tiwari A, Sathyaniranjan K, Chakrabarti K, Chattopadhyay D (2010) Culture independent molecular analysis of bacterial communities in the mangrove sediment of Sundarban, India. Saline Syst 6:1–5CrossRefPubMedPubMedCentralGoogle Scholar
  28. Good IJ (1953) The population frequencies of species and the estimation of population parameters. Biometrica 40:237–264CrossRefGoogle Scholar
  29. Gupta G, Parihar SS, Ahirwar NK, Snehi SK, Singh V (2015) Plant growth promoting rhizobacteria (PGPR): current and future prospects for development of sustainable agriculture. J Microb Biochem Technol 7:96–102Google Scholar
  30. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeont Electron 4(1):9–13Google Scholar
  31. Henderson PA, Seaby RMH (2014) Community analysis package version 5. Pisces Conservation Ltd, LymingtonGoogle Scholar
  32. Iverson V, Morris RM, Frazar CD, Berthiaume CT, Morales RL, Armbrust EV (2012) Untangling genomes from metagenomes: revealing an uncultured class of marine Euryarchaeota. Science 335:587–590CrossRefPubMedGoogle Scholar
  33. Krivushin K, Kondrashov F, Shmakova L, Tutukina M, Petrovskaya L, Rivkinaa E (2015) Two metagenomes from late Pleistocene northeast Siberian permafrost. Genome Announc 3(1):1380–1400CrossRefGoogle Scholar
  34. Langenheder S, Bulling MT, Solan M, Prosser JI (2010) Bacterial biodiversity–ecosystem functioning relations are modified by environmental complexity. PLoS ONE 5:e1083CrossRefGoogle Scholar
  35. Liszka M, Clark M, Schneider E, Clark DS (2012) Nature versus nurture: developing enzymes that function under extreme conditions. Ann Rev Chem Biomol Eng 3:77–102CrossRefGoogle Scholar
  36. López-López A, Yarza P, Richter M, Suárez-Suárez A et al (2010) Extremely halophilic microbial communities in anaerobic sediments from a solar saltern. Environ Microbiol Rep 2:258–271CrossRefPubMedGoogle Scholar
  37. Ma B, Gong J (2013) A meta-analysis of the publicly available bacterial and archaeal sequence diversity in saline soils. World J Microbiol Biotechnol 29:2325–2334CrossRefPubMedGoogle Scholar
  38. Malik KA, Bilal R, Mehnaz S, Rasool G, Mirza MS, Ali S (1997) Association of nitrogen-fixing, plant growth promoting rhizobacteria (PGPR) with kallar grass and rice. Plant Soil 194:37–44CrossRefGoogle Scholar
  39. Mirza BS, Muruganandam S, Meng X, Sorensen DL, Dupont RR, McLean JE (2014) Arsenic(V) reduction in relation to Iron(III) transformation and molecular characterization of the structural and functional microbial community in sediments of a basin-fill aquifer in Northern Utah. Appl Environ Microbiol 80:3198–3208CrossRefPubMedPubMedCentralGoogle Scholar
  40. Mukhtar S, Mirza MS, Awan HA, Maqbool A, Mehnaz S, Malik KA (2016) Microbial diversity and metagenomic analysis of the rhizosphere of para grass (Urochloa mutica) growing under saline conditions. Pak J Bot 48:779–791Google Scholar
  41. Mukhtar S, Ishaq A, Hassan S, Mehnaz S, Mirza MS, Malik KA (2017) Comparison of microbial communities associated with halophyte (Salsola stocksii) and non-halophyte (Triticum aestivum) using culture-independent approaches. Pol J Microbiol 66:375–386CrossRefGoogle Scholar
  42. Mukhtar S, Mirza MS, Mehnaz S, Mirza BS, Malik KA (2018) Diversity of Bacillus-like bacterial community in the rhizospheric and non-rhizospheric soil of halophytes (Salsola stocksii and Atriplex amnicola) and characterization of osmoregulatory genes in halophilic Bacilli. Can J Microbiol 64:567–579CrossRefPubMedGoogle Scholar
  43. Narasingarao P, Podell S, Ugalde JA, Brochier-Armanet C, Emerson JB, Brocks JJ, Heidelbert KB, Banfield JF, Allen EE (2012) De novo metagenomic assembly reveals abundant novel major lineage of Archaea in hypersaline microbial communities. ISME J 6:81–93CrossRefPubMedGoogle Scholar
  44. Naz I, Bano A, Hassan T (2009) Morphological, biochemical and molecular characterization of rhizobia from halophytes of Khewra salt range and Attock. Pak J Bot 41(6):3159–3168Google Scholar
  45. Niemho N, Suriyachadkun C, Tamura T, Thawai C (2013) Asanoa siamensis sp. nov., isolated from soil from a temperate peat swamp forest. Int J Syst Evol Microbiol 63(1):66–71CrossRefGoogle Scholar
  46. Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. USDA Circular, 939. USDA, Washington, DC, pp 1–19Google Scholar
  47. Pan Y, Cassman N, Hollander M, Mendes LW, Korevaar H, Geerts RHEM, van Veen JA, Kuramae EE (2014) Impact of long-term N, P, K, and NPK fertilization on the composition and potential functions of the bacterial community in grassland soil. FEMS Microbiol Ecol 90(1):195–205CrossRefPubMedGoogle Scholar
  48. Rengasamy R (2006) World salinization with emphasis on Australia. J Exp Bot 57:1017–1023CrossRefPubMedGoogle Scholar
  49. Rincon-Florez VA, Carvalhais LC, Schenck PM (2013) Culture-independent molecular tools for soil and rhizosphere microbiology. Diversity 5:581–612CrossRefGoogle Scholar
  50. Rolli E, Marasco R, Vigani G, Ettoumi B, Mapelli F et al (2015) Improved plant resistance to drought is promoted by the root-associated microbiome as a water stress-dependent trait. Environ Microbiol 17:316–331CrossRefPubMedGoogle Scholar
  51. Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88:1386–1394CrossRefPubMedGoogle Scholar
  52. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett W, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Gen Biol 12(6):R60CrossRefGoogle Scholar
  53. Tamaki H, Tanaka Y, Matsuzawa H, Muramatsu M, Meng XY et al (2011) Armatimonas rosea gen. nov., sp. nov., of a novel bacterial phylum, Armatimonadetes phyl. nov., formally called the candidate phylum OP10. Int J Syst Evol Microbiol 61:1442–1447CrossRefPubMedGoogle Scholar
  54. Taprig T, Akaracharanya A, Sitdhipol J, Visessanguan W, Tanasupawat S (2013) Screening and characterization of protease-producing Virgibacillus, Halobacillus and Oceanobacillus strains from Thai fermented fish. J Appl Pharm Sci 3:025–030Google Scholar
  55. Tripathi S, Kumari S, Chakraborty A, Gupta A, Chakrabarti K et al (2006) Microbial biomass and its activities in salt-affected coastal soils. Biol Fertil Soil 42:273–277CrossRefGoogle Scholar
  56. Tsuda K, Nagano H, Ando A, Shima J, Ogawa J (2015) Isolation and characterization of psychrotolerant endospore-forming Sporosarcina species associated with minced fish meat (surimi). Int J Food Microbiol 199:15–22CrossRefPubMedGoogle Scholar
  57. Vaisman N, Oren A (2009) Salisaeta longa gen. nov., sp. nov., a red, halophilic member of the Bacteroidetes. Int J Syst Evol Microbiol 59:2571–2574CrossRefPubMedGoogle Scholar
  58. Valenzuela-Encinas C, Neria-Gonzalez I, Alcantara-Hernandez RJ, Enriquez-Aragon JA, Estrada-Alvarado I, Hernandez-Rodriguez C, Dendooven L, Marsch R (2008) Phylogenetic analysis of the archaeal community in an alkaline-saline soil of the former lake Texcoco (Mexico). Extremophiles 12:247–254CrossRefPubMedGoogle Scholar
  59. Ventosa A, Mellado E, Sanchez-Porro C, Marquez MC (2008) Halophile and halotolerant microorganisms from soils. In: ds Dion P, Nautiyal CS (eds) Microbiology of extreme soils. Springer-Verlag, Berlin, pp 87–115CrossRefGoogle Scholar
  60. Wagg C, Bender SF, Widmer F, van der Heijden MG (2014) Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc Natl Acad Sci USA 111(14):5266–5270CrossRefPubMedGoogle Scholar
  61. Walkley A, Black IA (1934) An examination of Degtjareff method for determining soil organic matter and a proposed modification of the chromic acid titration method. Soil Sci 37:29–37CrossRefGoogle Scholar
  62. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267CrossRefPubMedPubMedCentralGoogle Scholar
  63. Wang Y, Sheng H, He Y, Wu J, Jiang Y, Tam N, Zhou H (2012) Comparison of the levels of bacterial diversity in freshwater, intertidal wetland, and marine sediments by using millions of illumina tags. Appl Environ Microbiol 78:8264–8271CrossRefPubMedPubMedCentralGoogle Scholar
  64. Yanagawa K, Breuker A, Schippers A, Nishizawa M, Ijiri A, Hirai M, Takaki Y (2014) Microbial community stratification controlled by the subsea floor fluid flow and geothermal gradient at the Iheya north hydrothermal field in the Mid-Okinawa trough (integrated ocean drilling program expedition 331). Appl Environ Microbiol 80(19):6126–6135CrossRefPubMedPubMedCentralGoogle Scholar
  65. Yancey PH (2005) Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J Exp Biol 208:2819–2830CrossRefPubMedGoogle Scholar
  66. Yousuf B, Sanadhya P, Keshri J. Jha B (2012) Comparative molecular analysis of chemolithoautitrophic bacterial diversity and community structure from coastal saline soils, Gujarat, India. BMC Microbiol 12:150CrossRefPubMedPubMedCentralGoogle Scholar
  67. Zhang Y, Cao C, Guo L, Wu Q, Cui Z (2015) Soil properties, bacterial community composition, and metabolic diversity responses to soil salinization of a semiarid grassland in northeast China. J Soil Water Conserv 70(2):110–120CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Salma Mukhtar
    • 1
  • Babur Saeed Mirza
    • 2
  • Samina Mehnaz
    • 1
  • Muhammad Sajjad Mirza
    • 3
  • Joan Mclean
    • 4
  • Kauser Abdulla Malik
    • 1
    Email author
  1. 1.Department of Biological SciencesForman Christian College (A Chartered University)LahorePakistan
  2. 2.Department of BiologyMissouri State UniversitySpringfieldUSA
  3. 3.Environmental Biotechnology DivisionNational Institute for Biotechnology and Genetic Engineering (NIBGE)FaisalabadPakistan
  4. 4.Utah Water Research Laboratory, Department of Civil and Environmental EngineeringUtah State UniversityLoganUSA

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