Microbial Ecology

, Volume 76, Issue 3, pp 782–790 | Cite as

Impacts of Phragmites australis Invasion on Soil Enzyme Activities and Microbial Abundance of Tidal Marshes

  • Sunghyun KimEmail author
  • Jiyoung Kang
  • J. Patrick Megonigal
  • Hojeong Kang
  • Jooyoung Seo
  • Weixin Ding
Soil Microbiology


The rapid expansion of Phragmites australis in brackish marshes of the East Coast of the USA has drawn much attention, because it may change vegetation diversity and ecosystem functions. In particular, higher primary production of Phragmites than that of other native species such as Spartina patens and Schoenoplectus americanus has been noted, suggesting possible changes in carbon storage potential in salt marshes. To better understand the long-term effect of the invasion of Phragmites on carbon storage, however, information on decomposition rates of soil organic matter is essential. To address this issue, we compared microbial enzyme activities and microbial functional gene abundances (fungi, laccase, denitrifier, and methanogens) in three depths of soils with three different plants in a brackish marsh in Maryland, USA. Laccase and phenol oxidase activities were measured to assess the decomposition potential of recalcitrant carbon while β-glucosidase activity was determined as proxy for cellulose decomposition rate. Microbial activities near the surface (0–15 cm) were the highest in Spartina-community sites followed by Phragmites- and Schoenoplectus-community sites. A comparison of stable isotopic signatures (δ13C and δ15N) of soils and plant leaves suggests that deep organic carbon in the soils mainly originated from Spartina, and only the surface soils may have been influenced by Phragmites litter. In contrast, fungal, laccase, and denitrifier abundances determined by real-time qPCR exhibited no discernible patterns among the surface soils of the three vegetation types. However, the abundance of methanogens was higher in the deep Phragmites-community soil. Therefore, Phragmites invasion will accelerate CH4 emission by greater CH4 production in deep soils with abundant methanogens, although enzymatic mechanisms revealed the potential for larger C accumulation by Phragmites invasion in salt marshes in the east coast of the USA.


Microbial activity Microbial abundance Salt marsh CH4 emission Phragmites invasion 


Funding Information

S. Kim was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science, and Technology (86457858).

Supplementary material

248_2018_1168_MOESM1_ESM.docx (2.7 mb)
ESM 1 (DOCX 2761 kb).


  1. 1.
    Mitra S, Wassmann R, Vlek P (2005) An appraisal of global wetland area and its organic carbon stock. Curr Sci 88:25–35Google Scholar
  2. 2.
    Deegan LA, Johnson DS, Warren RS (2012) Coastal eutrophication as a driver of salt marsh loss. Nature 490:388–392CrossRefPubMedGoogle Scholar
  3. 3.
    Kirwan ML, Guntenspergen GR, D’Alpaos A (2010) Limits on the adaptability of coastal marshes to rising sea level. Geophys Res Lett 37:23401CrossRefGoogle Scholar
  4. 4.
    Bardgett RD, Freeman C, Ostle N (2008) Microbial contributions to climate change through carbon cycle feedbacks. ISME J 2:805–814CrossRefPubMedGoogle Scholar
  5. 5.
    Chin Y, Aiken G, O’Loughlin E (1994) Molecular weight, polydispersity, and spectroscopic properties of aquatic humic substances. Environ Sci Technol 28:1853–1858CrossRefPubMedGoogle Scholar
  6. 6.
    Baldrian P (2006) Fungal laccases—occurrence and properties. FEMS Microbiol Rev 30:215–242CrossRefPubMedGoogle Scholar
  7. 7.
    Freeman C, Ostle N, Kang H (2001) An enzymic ‘latch’ on a global carbon store. Nature 409:149CrossRefPubMedGoogle Scholar
  8. 8.
    Fourqurean J, Duarte C, Kennedy H (2012) Seagrass ecosystems as a globally significant carbon stock. Nat Geosci 5:505–509CrossRefGoogle Scholar
  9. 9.
    Saltonstall K (2002) Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America. Proc Natl Acad Sci U S A 99:2445–2449CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Artigas F, Shin JY, Hobble C, Marti-Donati A, Schafer K, Pechmann I (2015) Long term carbon storage potential and CO2 sink strength of a restored salt marsh in New Jersey. Agric For Meteorol 200:313–321CrossRefGoogle Scholar
  11. 11.
    Uddin MN, Robinson RW, Caridi D, Harun AY (2013) Is phytotoxicity of Phragmites australis residue influenced by decomposition condition, time and density? Mar Freshw ResGoogle Scholar
  12. 12.
    Neubauer and Megonigal (2015) Moving beyond global warming potentials to quantify the climatic role of ecosystems. Ecosystems 18:1000–1013CrossRefGoogle Scholar
  13. 13.
    Bridgham SD, Megonigal JP, Keller JK (2006) The carbon balance of North American wetlands. Wetlands 26(4):889–916CrossRefGoogle Scholar
  14. 14.
    Dar SA, Kleerebezem R, Stams AJM, Kuenen JG, Muyzer G (2008) Competition and coexistence of sulfate-reducing bacteria, acetogens and methanogens in a lab-scale anaerobic bioreactor as affected by changing substrate to sulfate ratio. Appl Microbiol Biotechnol 78(6):1045–1055CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Poffenbarger HJ, Needleman BA, Megonigal JP (2011) Salinity influence on methane emissions from tidal marshes. Wetlands 31:831–842CrossRefGoogle Scholar
  16. 16.
    Rothman E, Bouchard V (2007) Regulation of carbon processes by macrophyte species in a Great Lakes coastal wetland. Wetlands 27:1134–1143CrossRefGoogle Scholar
  17. 17.
    Mozdzer T, Megonigal P (2013) Increased methane emissions by an introduced Phragmites australis lineage under global change. Wetlands 33:609–615CrossRefGoogle Scholar
  18. 18.
    Mueller P, Hager R, Meschter J, Mozdzer T, Langley J, Jensen K, Megonigal JP (2016) Complex invader-ecosystem interactions and seasonality mediate the impact of non-native Phragmites on CH4 emissions. Biol Invasions.
  19. 19.
    Martin R, Moseman-Valtierra S (2015) Greenhouse gas fluxes vary between Phragmites Australis and native vegetation zones in coastal wetlands along a salinity gradient. Wetlands 35:1102–1031CrossRefGoogle Scholar
  20. 20.
    Caplan JS, Hager RN, Megonigal JP, Mozdzer TJ (2015) Global change accelerates carbon assimilation by a wetland ecosystem engineer. Environ Res Lett 10:115006CrossRefGoogle Scholar
  21. 21.
    McCormick MK, Kettenring KM, Baron HM, Whigham DF (2010) Extent and reproductive mechanisms of Phragmites australis spread in brackish wetlands in Chesapeake Bay, Maryland (USA). Wetlands 30:67–74CrossRefGoogle Scholar
  22. 22.
    Carney KM, Hungate BA, Drake BG, Megonigal JP (2007) Altered soil microbial community at elevated CO2 leads to loss of soil carbon. Proc Natl Acad Sci 104:4990–4995CrossRefPubMedGoogle Scholar
  23. 23.
    Sinsabaugh RL, Carreiro MM, Repert DA (2002) Allocation of extracellular enzymatic activity in relation to litter composition, N deposition, and mass loss. Biogeochemistry 60:1–24CrossRefGoogle Scholar
  24. 24.
    Pind A, Freeman C, Lock MA (1994) Enzymic degradation of phenolic materials in peatlands—measurement of phenol oxidase activity. Plant Soil 159:227–231CrossRefGoogle Scholar
  25. 25.
    Wright AL, Reddy KR (2001) Phosphorous loading effects on extracellular enzyme activity in Everglades wetland soils. Soil Sci Soc Am J 53:1723–1729Google Scholar
  26. 26.
    Matsumura E, Shin T, Murao S, Yamamoto E, Kawano T (1987) New enzymatic colorimetric reactions of benzoic acid derivatives with ABTS 2, 20-azinobis-3-ethylbenzthiazoline-6-sulfonic acid diammonium salt in the presence of laccase. Agric Biol Chem 51:2743–2750Google Scholar
  27. 27.
    White T, Bruns T, Lee S, Taylor J, Innis M, Gelfand D, Sninsky J (1990) PCR protocols: a guide to methods and applications. Academic Press, New YorkGoogle Scholar
  28. 28.
    Luis P, Walther G, Jellner H, Martin F, Buscot F (2004) Diversity of laccase genes from basidiomycetes in a forest soil. Soil Biol Biochem 36:1025–1036CrossRefGoogle Scholar
  29. 29.
    Lauber CL, Sinsabaugh RL (2009) Laccase gene composition and relative abundance in oak forest soil is not affected by short-term nitrogen fertilization. Soil Microbiol 57:50–57Google Scholar
  30. 30.
    Sinsabaugh RL, Moorhead DL (1994) Resource allocation to extracellular enzyme production: a model for nitrogen and phosphorus control of litter decomposition. Soil Biol Biochem 26:1305–1311CrossRefGoogle Scholar
  31. 31.
    Luesters T, Friedrich NW (2003) Evaluation of PCR amplification bias by terminal restriction fragment length polymorphism analysis of small-subunit rRNA and mcrA genes by using defined template mixtures of methanogenic pure cultures and soil DNA extracts. Appl Environ Microbiol 69:32–326Google Scholar
  32. 32.
    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 69:3249–3560Google Scholar
  33. 33.
    Chimney MJ, Pietro KC (2006) Decomposition of macrophyte litter in a subtropical constructed wetland in South Florida. Ecol Eng 27:301–321CrossRefGoogle Scholar
  34. 34.
    Kennedy E, Leff LG, de Szalay FA (2012) Herbiciding Phragmites australis: effects on litter decomposition, microbial biomass, and macroinvertebrate communities. Fundam Appl Limnol 180:309–319CrossRefGoogle Scholar
  35. 35.
    Findlay SEG, Dye S, Kuehn KA (2002) Microbial growth and nitrogen retention in litter of Phragmites australis compared to Typha angustifolia. Wetlands 22:616–625CrossRefGoogle Scholar
  36. 36.
    Kuehn KA, Steiner D, Gessner MO (2004) Diel mineralization patterns of standing dead plant litter: implications for CO2 flux from wetlands. Ecology 85:2504–2518CrossRefGoogle Scholar
  37. 37.
    Agoston-Szabo E, Dinka M (2008) Decomposition of Typha angustifolia and Phragmites australis in the littoral zone of a shallow lake. Biologia 63:1104–1110CrossRefGoogle Scholar
  38. 38.
    Duke ST (2012) Effects of invasion by the common reed (Phragmites australis) on carbon transformations in a Great Lakes Marsh. Master’s theses. Eastern Michigan UniversityGoogle Scholar
  39. 39.
    Bernal B, Megonigal JP, Mozdzer T (2016) An invasive wetland grass primes deep soil carbon pools. Glob Chang Biol.
  40. 40.
    Cheng X, Peng R, Chen J (2007) CH4 and N2O emissions from Spartina alterniflora and Phragmites australis in experimental mesocosms. Chemosphere 68:420–427CrossRefPubMedGoogle Scholar
  41. 41.
    Fierer N, Schimel J, Holden P (2003) Variations in microbial community composition through two soil depth profiles. Soil Biol Biochem 35:167–176CrossRefGoogle Scholar
  42. 42.
    Freeman C, Nevison GB, Kang H, Hughes S, Reynolds B, Hudson JA (2002) Contrasted effects of simulated drought on the production and oxidation of methane in a mid-Wales wetlands. Soil Biol Biochem 34:61–67CrossRefGoogle Scholar
  43. 43.
    Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523CrossRefGoogle Scholar
  44. 44.
    Moore GE, Burdick DM, Peter CR, Keirstead DR (2012) Belowground biomass of Phragmites australis in coastal marshes. Northeast Nat 19:611–626CrossRefGoogle Scholar
  45. 45.
    Whiting GJ, Chanton JP (1993) Primary production control of methane emission from wetlands. Nature 364:794–795CrossRefGoogle Scholar
  46. 46.
    Kankaala P, Ojala A, Kaki T (2004) Temporal and spatial variation in methane emissions from a flooded transgression shore of a boreal lake. Biogeochemistry 68:297–311CrossRefGoogle Scholar
  47. 47.
    Kim J, Lee S, Jang I, Jeong S, Kang H (2015) Can abundance of methanogen be a good indicator for CH4 flux in soil ecosystems? Environ Geochem Health 37:1007–1015CrossRefPubMedGoogle Scholar
  48. 48.
    Megonigal JP, Schlesinger WH (2002) Methane-limited methanotrophy in tidal freshwater swamps. Glob Biogeochem Cycles 16:1088CrossRefGoogle Scholar
  49. 49.
    Shackle VJ, Freeman C, Reynolds (2000) Carbon supply and the regulation of enzyme activity in constructed wetlands. Soil Biol Biochem 32:1935–1940CrossRefGoogle Scholar
  50. 50.
    Ma WK, Schautz A, Fishback LE, Bedard-Haughn A, Farrell RE, Siciliano SD (2007) Assessing the potential of ammonia oxidizing bacteria to produce nitrous oxide in soils of high arctic lowland ecosystem on Devon Island, Canada. Soil Biol Biochem 39:2001–2013CrossRefGoogle Scholar
  51. 51.
    Dowrick DJ, Hughes S, Freeman C, Lock MA, Reynolds B, Hudson JA (1999) Nitrous oxide emissions from a gully mire in mid-Wales, UK, under simulated summer drought. Biogeochemistry 44:151–162Google Scholar
  52. 52.
    Kim SY, Lee SH, Freeman C, Fenner N, Kang H (2008) Comparative analysis of soil microbial communities and their responses to the short-term drought in bog, fen, and riparian wetlands. Soil Biol Biochem 40:2874–2880CrossRefGoogle Scholar
  53. 53.
    Palmer K, Horn MA (2012) Actinobacterial nitrate reducers and proteobacterial denitrifiers are abundant in N2O-metabolizing palsa peat. Appl Environ Microbiol 78:5584–5596CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Sunghyun Kim
    • 1
    • 2
    Email author
  • Jiyoung Kang
    • 3
  • J. Patrick Megonigal
    • 1
  • Hojeong Kang
    • 4
  • Jooyoung Seo
    • 4
  • Weixin Ding
    • 2
  1. 1.Smithsonian Environmental Research CenterEdgewaterUSA
  2. 2.State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil ScienceChinese Academy of SciencesNanjingChina
  3. 3.Benjamin Franklin CollegeYale UniversityNew HavenUSA
  4. 4.School of Civil and Environmental EngineeringYonsei UniversitySeoulSouth Korea

Personalised recommendations