Influences of Different Halophyte Vegetation on Soil Microbial Community at Temperate Salt Marsh

Plant Microbe Interactions

Abstract

Salt marshes are transitional zone between terrestrial and aquatic ecosystems, occupied mainly by halophytic vegetation which provides numerous ecological services to coastal ecosystem. Halophyte-associated microbial community plays an important role in the adaptation of plants to adverse condition and also affected habitat characteristics. To explore the relationship between halophytes and soil microbial community, we studied the soil enzyme activities, soil microbial community structure, and functional gene abundance in halophytes- (Carex scabrifolia, Phragmites australis, and Suaeda japonica) covered and un-vegetated (mud flat) soils at Suncheon Bay, South Korea. Higher concentrations of total, Gram-positive, Gram-negative, total bacterial, and actinomycetes PLFAs (phospholipid fatty acids) were observed in the soil underneath the halophytes compared with mud flat soil and were highest in Carex soil. Halophyte-covered soils had different microbial community composition due to higher abundance of Gram-negative bacteria than mud flat soil. Similar to PLFA concentrations, the increased activities of β-glucosidase, cellulase, phosphatase, and sulfatase enzymes were observed under halophyte soil compared to mud flat soil and Carex exhibited highest activities. The abundance of archaeal 16S rRNA, fungal ITS, and denitrifying genes (nirK, nirS, and nosZ) were not influenced by the halophytes. Abundance bacterial 16S rRNA and dissimilatory (bi)sulfite (dsrA) genes were highest in Carex-covered soil. The abundance of functional genes involved in methane cycle (mcrA and pmoA) was not affected by the halophytes. However, the ratios of mcrA/pmoA and mcrA/dsrA increased in halophyte-covered soils which indicate higher methanogenesis activities. The finding of the study also suggests that halophytes had increased the microbial and enzyme activities, and played a pivotal role in shaping microbial community structure.

Keywords

Enzymes Functional gene abundance Microbial community PLFA Salt marsh 

Notes

Acknowledgements

This work was supported by Brainpool fellowship of the Korean Federation of Science and Technology (KOFST). This paper was studied with the support of the Korean Ministry of Science, ICT and Future Planning (MSIP) and National Research Foundation of Korea (20110030040 and 2015K2A2A2002194), and Korean Ministry of Education (SGER; 2016R1D1A1A02937049).

Supplementary material

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ESM 1(DOCX 22.6 kb)
248_2017_1083_MOESM2_ESM.docx (13 kb)
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References

  1. 1.
    Pendleton L, Donato D, Murray B, Crooks S, Jenkins WA, Sifleet S, Craft C, Fourqurean J, Kauffman JB, Marba N, Megonigal P, Pidgeon E, Herr D, Gordon D, Baldera A (2012) Estimating global “blue carbon” emissions from conversion and degradation of vegetated coastal ecosystems. PLoS One 7:e43542. https://doi.org/10.1371/journal.pone.0043542 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Boorman LA (1999) Salt marshes-present function and future change. Mangrove Salt Marshes 3:227–241. https://doi.org/10.1023/A:1009998812838 CrossRefGoogle Scholar
  3. 3.
    Shepard CC, Crain CM, Beck MW (2011) The protective role of coastal marshes: a systematic review and meta-analysis. PLoS One 6(11):e27374. https://doi.org/10.1371/journal.pone.0027374 CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Glenn EP, Brown JJ, Blumwald E (1999) Salt tolerance and crop potential of halophytes. Crit Rev Plant Sci 18:227–255CrossRefGoogle Scholar
  5. 5.
    Hasanuzzaman M, Nahar K, Alam MM, Bhowmik PC, Hossain MA, Rahman MM, Prasad MNV, Ozturk M, Fujita M (2014) Potential use of halophytes to remediate saline soils. BioMed Res Inter 2014:589341, 12 pages, 2014. https://doi.org/10.1155/2014/589341 Google Scholar
  6. 6.
    Simas T, Nunes JP, Ferreira JG (2001) Effects of global climate change on coastal salt marshes. Ecol Model 139:1–15. https://doi.org/10.1016/S0304-3800(01)00226-5 CrossRefGoogle Scholar
  7. 7.
    Pennings SC, Bertness MD (2001) Salt marsh communities. In: Bertness MD, Gaines SD, Hay M (eds) Marine community ecology. Sinauer Associates, Sunderland, pp. 289–316Google Scholar
  8. 8.
    Duarte C, Losada IJ, Hendriks IE, Mazarrasa I, Marbà N (2013) The role of coastal plant communities for climate change mitigation and adaptation. Nat Clim Chang 3:961–968. https://doi.org/10.1038/nclimate1970 CrossRefGoogle Scholar
  9. 9.
    Miki T, Ushio M, Fukui S, Kondoh M (2010) Functional diversity of microbial decomposers facilitates plant coexistence in a plant-microbe-soil feedback model. Proc Natl Acad Sci 107:14251–14256. https://doi.org/10.1073/pnas.0914281107 CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Ai C, Liang G, Sun J, Wang X, Zhou W (2012) Responses of extracellular enzyme activities and microbial community in both the rhizosphere and bulk soil to long-term fertilization practices in a fluvo-aquic soil. Geoderma 173-174:330–338. https://doi.org/10.1016/j.geoderma.2011.07.020 CrossRefGoogle Scholar
  11. 11.
    Chaudhary DR, Gautam RK, Yousuf B, Mishra A, Jha B (2015) Nutrients, microbial community structure and functional gene abundance of rhizosphere and bulk soils of halophytes. Appl Soil Ecol 91:16–26. https://doi.org/10.1016/j.apsoil.2015.02.003 CrossRefGoogle Scholar
  12. 12.
    Kamer M, Rassoulzadegan F (1995) Extracellular enzyme activity: indications for high short-term variability in a coastal marine ecosystem. Microb Ecol 30:143–156. https://doi.org/10.1007/BF00172570 CrossRefPubMedGoogle Scholar
  13. 13.
    Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13. https://doi.org/10.1111/j.1574-6941.2009.00654.x CrossRefPubMedGoogle Scholar
  14. 14.
    Dennis PG, Miller AJ, Hirsch PR (2010) Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? FEMS Microbiol Ecol 72:313–327. https://doi.org/10.1111/j.15746941.2010.00860.x CrossRefPubMedGoogle Scholar
  15. 15.
    Rietl AJ, Overlander ME, Nyman AJ, Jackson CR (2016) Microbial community composition and extracellular enzyme activities associated with Juncus roemerianus and Spartina alterniflora vegetated sediments in Louisiana saltmarshes. Microb Ecol 71:290–303. https://doi.org/10.1007/s00248-015-0651-2 CrossRefPubMedGoogle Scholar
  16. 16.
    Barness G, Zaragoza SR, Shmueli I, Steinberger Y (2009) Vertical distribution of a soil microbial community as affected by plant ecophysiological adaptation in a desert system. Microb Ecol 57:36–49. https://doi.org/10.1007/s00248-008-9396-5 CrossRefPubMedGoogle Scholar
  17. 17.
    Brimecombe MJ, De Leij FA, Lynch JA (2001) The effect of root exudates on rhizosphere microbial populations. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere: biochemistry and organic substances at the soil-plant interface. Marcel Dekker Inc, New York, pp. 95–104Google Scholar
  18. 18.
    Mishra RR, Swain MR, Dangar TK, Thatoi H (2012) Diversity and seasonal fluctuation of predominant microbial communities in Bhitarkanika, a tropical mangrove ecosystem in India. Rev Biol Trop 60:909–924PubMedGoogle Scholar
  19. 19.
    Kristensen E, Mangion P, Tang M, Flindt MR, Holmer M, Ulomi S (2011) Microbial carbon oxidation rates and pathways in sediments of two Tanzanian mangrove forests. Biogeochemisty 103:143–158. https://doi.org/10.1007/s10533-010-9453-2 CrossRefGoogle Scholar
  20. 20.
    Laverman AM, Pallud C, Abell J, Van Cappellen P (2012) Comparative survey of potential nitrate and sulfate reduction rates in aquatic sediments. Geochim Cosmochim Acta 77:474–488. https://doi.org/10.1016/j.gca.2011.10.033 CrossRefGoogle Scholar
  21. 21.
    Kondo R, Shigematsu K, Butani J (2004) Rapid enumeration of sulphate-reducing bacteria from aquatic environments using real-time PCR. Plankton Benthos Res 3:180–183CrossRefGoogle Scholar
  22. 22.
    Kondo R, Nedwell DB, Purdy KJ, Silva SQ (2004) Detection and enumeration of sulphate-reducing bacteria in estuarine sediments by competitive PCR. Geomicrobiol J 21(3):145–157. https://doi.org/10.1080/01490450490275307 CrossRefGoogle Scholar
  23. 23.
    Bahr M, Crump BC, Klepac-Ceraj V, Teske A, Sogin ML, Hobbie JE (2005) Molecular characterization of sulfate-reducing bacteria in a New England salt marsh. Environ Microbiol 7:1175–1185. https://doi.org/10.1111/j.1462-2920.2005.00796.x CrossRefPubMedGoogle Scholar
  24. 24.
    Braker G, Zhou J, Wu L, Devol AH, Tiedje JM (2000) Nitrite reductase genes (nirK and nirS) as functional markers to investigate diversity of denitrifying bacteria in Pacific Northwest marine sediment communities. Appl Environ Microbiol 66:2096–2104. https://doi.org/10.1128/AEM.66.5.2096-2104.2000 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Graves CJ, Makrides EJ, Schmidt VT, Giblin AE, Cardon ZG, Rand DM (2016) Functional responses of salt marsh microbial communities to long-term nutrient enrichment. Appl Environ Microbiol 82:2862–2871. https://doi.org/10.1128/AEM.03990-15 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Friedrich MW (2005) Methyl-coenzyme M reductase genes: unique functional markers for methanogenic and anaerobic methane-oxidizing archaea. Methods Enzymol 397:428–442. https://doi.org/10.1016/S00766879(05)97026-2 CrossRefPubMedGoogle Scholar
  27. 27.
    Dumont MG, Murrell JC (2005) Community-level analysis: key genes of aerobic methane oxidation. Methods Enzymol 397:413–427. https://doi.org/10.1016/S0076-6879(05)97025-0 CrossRefPubMedGoogle Scholar
  28. 28.
    Saltonstall K (2002) Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America. Proc Natl Acad Sci 99:2445–2449. https://doi.org/10.1073/pnas.03247799 CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Zeleke J, Sheng Q, Wang J, Huang M, Xia F, Wu J, Quan Z (2013) Effects of Spartina alterniflora invasion on the communities of methanogens and sulfate-reducing bacteria in estuarine march sediments. Front Microbiol 4:Article 243. https://doi.org/10.3389/fmicb.2013.00243 CrossRefPubMedGoogle Scholar
  30. 30.
    Yuan J, Ding W, Liu D, Kang H, Freeman C, Xiang J, Lin Y (2015) Exotic Spartina alterniflora invasion alters ecosystem-atmosphere exchange of CH4 and N2O and carbon sequestration in a coastal salt marsh in China. Glob Chang Biol 21:1567–1580. https://doi.org/10.1111/gcb.12797 CrossRefPubMedGoogle Scholar
  31. 31.
    Bardgett RD, Hobbs PJ, Frostagård A (1996) Changes in soil fungal: bacterial biomass following reduction in the intensity of management of an upland grassland. Biol Fertil Soils 22:261–264. https://doi.org/10.1007/BF00382522 CrossRefGoogle Scholar
  32. 32.
    Frostegård A, Bååth E, Tunlid A (1993) Shifts in the structure of soil microbial communities in limed forests as revealed by phospholipid fatty acid analysis. Soil Biol Biochem 25:723–730. https://doi.org/10.1016/0038-0717(93)90113-P CrossRefGoogle Scholar
  33. 33.
    Zelles L (1996) Fatty acid patterns of microbial phospholipids and lipopolysaccharides. In: Schinner F, Ohlinger R, Kandeler E, Margesin R (eds) Methods in soil biology. Springer-Verlag, Berlin, pp. 80–92Google Scholar
  34. 34.
    Kaur A, Chaudhary A, Kaur A, Choudhary R, Kaushik R (2005) Phospholipid fatty acid- A bioindicator of environment monitoring and assessment in soil ecosystem. Curr Sci 89:1103–1112Google Scholar
  35. 35.
    Kang H, Freeman C (1999) Phosphatase and arylsulphatase activities in wetland soils: annual variation and controlling factors. Soil Biol Biochem 31:449–454. https://doi.org/10.1016/S0038-0717(98)00150-3 CrossRefGoogle Scholar
  36. 36.
    Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrant E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp. 115–175Google Scholar
  37. 37.
    Takai K, Horikoshi K (2000) Rapid detection and quantification of members of the archaeal community by quantitative PCR using fluorogenic probes. Appl Environ Microbiol 66:5066–5072CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118CrossRefPubMedGoogle Scholar
  39. 39.
    White TJ, Bruns TD, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press Inc, New York, pp. 315–324Google Scholar
  40. 40.
    Steinberg LM, Regan JM (2008) Phylogenetic comparison of the methanogenic communities from an acidic, oligotrophic fen and an anaerobic digester treating municipal wastewater sludge. Appl Environ Microbiol 74:6663–6671. https://doi.org/10.1128/AEM.00553-08 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Hales BA, Edwards C, Ritchie DA, Hall G, Pickup RW, Saunders JR (1996) Isolation and identification of methanogen-specific DNA from blanket bog peat by PCR amplification and sequence analysis. Appl Environ Microbiol 62:668–675PubMedPubMedCentralGoogle Scholar
  42. 42.
    Holmes AJ, Costello A, Lidstrom ME, Murrell JC (1995) Evidence that participate methane monooxygenase and ammonia monooxygenase may be evolutionarily related. FEMS Microbiol Lett 132:203–208CrossRefPubMedGoogle Scholar
  43. 43.
    Costello AM, Lidstrom ME (1999) Molecular characterization of functional and phylogenetic genes from natural populations of methanotrophs in lake sediments. Appl Environ Microbiol 65:5066–5074PubMedPubMedCentralGoogle Scholar
  44. 44.
    Liu X, Tiquia SM, Holguin G, Wu L, Nold SC, Devol AH, Luo K, Palumbo AV, Tiedje JM, Zhou J (2003) Molecular diversity of denitrifying genes in continental margin sediments within the oxygen-deficient zone off the Pacific coast of Mexico. Appl Environ Microbiol 69:3549–3560. https://doi.org/10.1128/AEM.69.6.3549-3560.2003 CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Braker G, Fesefeldt A, Witzel KP (1998) Development of PCR primer systems for amplification of nitrite reductase genes (nirK and nirS) to detect denitrifying bacteria in environmental samples. Appl Environ Microbiol 64:3769–3775PubMedPubMedCentralGoogle Scholar
  46. 46.
    Henry S, Baudoin E, López-Gutiérrez JC, Martin-Laurent F, Brauman A, Philippot L (2004) Quantification of denitrifying bacteria in soils by nirK gene targeted real-time PCR. J Microbiol Methods 59:327–335. https://doi.org/10.1016/j.mimet.2004.07.002 CrossRefPubMedGoogle Scholar
  47. 47.
    Rich J, Heichen R, Bottomley P, Cromack Jr K, Myrold D (2003) Community composition and functioning of denitrifying bacteria from adjacent meadow and forest soils. Appl Environ Microbiol 69:5974–5982. https://doi.org/10.1128/AEM.69.10.5974-5982.2003 CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    McCune B, Mefford MJ (2006) PC-ORD. Multivariate analysis of ecological data, Version 5. MjM Software, Gleneden Beach, Google Scholar
  49. 49.
    Oliveira V, Santos AL, Coelho F, Gomes NCM, Silva H, Almeida A, Cunha  (2010) Effects of monospecific banks of salt marsh vegetation on sediment bacterial communities. Microb Ecol 60:167–179. https://doi.org/10.1007/s00248-010-9678-6 CrossRefPubMedGoogle Scholar
  50. 50.
    Wang M, Chen JK, Li B (2007) Characterization of bacterial community structure and diversity in rhizosphere soils of three plants in rapidly changing salt marshes using 16S rDNA. Pedosphere 17:545–556. https://doi.org/10.1016/S1002-0160(07)60065-4 CrossRefGoogle Scholar
  51. 51.
    Chaudhary DR, Rathore AP, Kumar R, Jha B (2017) Spatial and halophytes associated microbial communities in intertidal coastal region of India. Int J Phytoremediation 19:478–489. https://doi.org/10.1080/15226514.2016.1244168 CrossRefPubMedGoogle Scholar
  52. 52.
    Szymańska S, Płociniczak T, Piotrowska-Seget Z, Hrynkiewicz K (2016) Endophytic and rhizosphere bacteria associated with the roots of the halophyte Salicornia europaea L.—community structure and metabolic potential. Microbiol Res 192:37–51. https://doi.org/10.1016/j.micres.2016.05.012 CrossRefPubMedGoogle Scholar
  53. 53.
    Esperschütz J, Buegger F, Winkler JB, Munch JC, Schloter M, Gattinger A (2009) Microbial response to exudates in the rhizosphere of young beech trees (Fagus sylvatica L.) after dormancy. Soil Biol Biochem 41:1976–1985. https://doi.org/10.1016/j.soilbio.2009.07.002 CrossRefGoogle Scholar
  54. 54.
    Oremland RS, Marsh LM, Polcin S (1982) Methane production and simultaneous sulphate reduction in anoxic, salt marsh sediments. Nature 296:143–145CrossRefGoogle Scholar
  55. 55.
    Winfrey MR, Ward DM (1983) Substrates for sulfate reduction and methane production in intertidal sediments. Appl Environ Microbiol 45:193–199PubMedPubMedCentralGoogle Scholar
  56. 56.
    Oremland RS, Polcin S (1982) Methanogenesis and sulfate reduction: competitive and noncompetitive substrates in estuarine sediments. Appl Environ Microbiol 44:1270–1276PubMedPubMedCentralGoogle Scholar
  57. 57.
    Freitag TE, Toet S, Ineson P, Prosser JI (2010) Links between methane flux and transcriptional activities of methanogens and methane oxidizers in a blanket peat bog. FEMS Microbiol Ecol 73:157–165. https://doi.org/10.1111/j.1574-6941.2010.00871.x PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  1. 1.Marine Biotechnology and Ecology DivisionCentral Salt and Marine Chemicals Research Institute (CSIR)BhavnagarIndia
  2. 2.Academy of Scientific and Innovative Research (AcSIR)CSIRNew DelhiIndia
  3. 3.School of Civil and Environmental EngineeringYonsei UniversitySeoulSouth Korea

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