Skip to main content

Advertisement

SpringerLink
Log in

Changes in Archaeal Community and Activity by the Invasion of Spartina anglica Along Soil Depth Profiles of a Coastal Wetland

  • Soil Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Invasion of Spartina spp. in tidal salt marshes may affect the function and characteristics of the ecosystem. Previous studies reported that the invasion alters biogeochemical and microbial processes in marsh ecosystems, yet our knowledge of changing archaeal community due to the invasion is still limited, whereas archaeal communities play a pivotal role in biogeochemical cycles within highly reduced marsh soils. In this study, we aimed to illustrate the influences of the Spartina anglica invasion on soil archaeal community and the depth profile of the influences. The relative abundance of archaeal phyla demonstrated that the invasion substantially shifted the characteristics of tidal salt marsh from marine to terrestrial soil only in surface layer, while the influences indirectly propagated to the deeper soil layer. In particular, two archaeal phyla, Asgardaeota and Diapherotrites, were strongly influenced by the invasion, indicating a shift from marine to terrestrial archaeal communities. The shifts in soil characteristics spread to the deeper soil layer that results in indirect propagation of the influences of the invasion down to the deeper soil, which was underestimated in previous studies. The changes in the concentration of dissolved organic carbon and salinity were the substantial regulating factors for that. Therefore, changes in biogeochemical and microbial characteristics in the deep soil layer, which is below the root zone of the invasive plant, should be accounted for a more accurate illustration of the consequences of the invasion.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data Availability

All data appeared in this manuscript will be available upon request.

References

  1. 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

    Article  PubMed  Google Scholar 

  2. Kerr DW, Hogle IB, Ort BS, Thornton WJ (2016) A review of 16 years of Spartina management in the San Francisco Estuary. Biol Invasions 18:2247–2266. https://doi.org/10.1007/s10530-016-1178-2

    Article  Google Scholar 

  3. Strong DR, Ayres DA (2016) Control and consequences of Spartina spp. invasions with focus upon San Francisco Bay. Biol Invasions 18:2237–2246. https://doi.org/10.1007/s10530-015-0980-6

    Article  Google Scholar 

  4. Nehring S, Hesse KJ (2008) Invasive alien plants in marine protected areas: the Spartina anglica affair in the European Wadden Sea. Biol Invasions 10:937–950. https://doi.org/10.1007/s10530-008-9244-z

    Article  Google Scholar 

  5. Kim E-K, Kil J, Joo Y-K, Jung Y-S (2015) Distribution and botanical characteristics of unrecorded alien weed Spartina anglicai in Korea. Weed Turf Sci 4:65–70. https://doi.org/10.5660/WTS.2015.4.1.65

    Article  Google Scholar 

  6. Kim J-S (2016) A research review for establishing effective management practices of the highly invasive cordgrass (Spartina spp.). Weed Turf Sci 5:111–125. https://doi.org/10.5660/WTS.2016.5.3.111

    Article  Google Scholar 

  7. KOEM (2018). Korea Marine Environment Management Corporation Marine Ecosystem Restoration. https://www.koem.or.kr/site/koem/04/10401020000002019051004.jsp

  8. Aberle B (1990) The biology control and eradication of introduced Spartina (cordgrass) worldwide and recommendations for its control in Washington. Draft report to Washington Department of Natural Resources, Olympia. https://www.cabi.org/isc/abstract/20067204288

  9. Hill MI (n.d.) Population differentiation in Spartina in the Dee estuary - common garden and reciprocal transplant experiments. In: Gray AJ, Benham PEM (eds) Spartina anglica - A research review. Institute of Terrestrial Ecology Research Publlication 2 HMSO, London, pp 15–19. http://nora.nerc.ac.uk/id/eprint/7639/1/Spartina_Anglica.pdf

  10. Chmura GL, Anisfeld SC, Cahoon DR, Lynch JC (2003) Global carbon sequestration in tidal, saline wetland soils. Global Biogeochem Cycles 17:1111. https://doi.org/10.1029/2002GB001917

    Article  CAS  Google Scholar 

  11. Bernal B, Megonigal JP, Mozdzer TJ (2017) An invasive wetland grass primes deep soil carbon pools. Glob Chang Biol 23:2104–2116. https://doi.org/10.1111/gcb.13539

    Article  PubMed  Google Scholar 

  12. Kim J, Chaudhar DR, Lee J, Byun C, Ding W, Kwon B-O, Khim JS, Kang H (2020) Microbial mechanism for enhanced methane emission in deep soil layer of Phragmites-introduced tidal marsh. Environ Int 134:105251. https://doi.org/10.1016/j.envint.2019.105251

    Article  CAS  PubMed  Google Scholar 

  13. Kim J, Lee J, Yun J, Yang Y, Ding W, Yuan J, Kang H (2020) Mechanisms of enhanced methane emission due to introduction of Spartina anglica and Phragmites australis in a temperate tidal salt marsh. Ecol Eng 153:105905. https://doi.org/10.1016/j.ecoleng.2020.105905

    Article  Google Scholar 

  14. An S-U, Cho H, Jung U-J, Kim B, Lee H, Hyun J-H (2020) Invasive Spartina anglica greatly alters the rates and pathways of organic carbon oxidation and associated microbial communities in an intertidal wetland of the Han River Estuary. Yellow Sea Front Mar Sci 7:59. https://doi.org/10.3389/fmars.2020.00059

    Article  Google Scholar 

  15. Kim J, Lee J, Yang Y, Yun J, Ding X, Yuan J, Khim JS, Kwon B-O, Kang H (2021) Microbial decomposition of soil organic matter determined by edaphic characteristics of mangrove forests in East Asia. Sci Total Environ 763:142972. https://doi.org/10.1016/j.scitotenv.2020.142972

    Article  CAS  PubMed  Google Scholar 

  16. Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363. https://doi.org/10.1111/j.1461-0248.2008.01250.x

    Article  PubMed  Google Scholar 

  17. Dawson W, Rohr RP, van Kleunen M, Fischer M (2012) Alien plant species with a wider global distribution are better ableto capitalize on increased resource availability. New Phytol 194:859–867. https://doi.org/10.1111/j.1469-8137.2012.04104.x

    Article  PubMed  Google Scholar 

  18. Mozdzer TJ, Megonigal JP (2013) Increased methane emissions by an introduced Phragmites australis lineage under global change. Wetlands 33:609–615. https://doi.org/10.1007/s13157-013-0417-x

    Article  Google Scholar 

  19. Emery HE, Fulweiler RW (2014) Spartina alterniflora and invasive Phragmites australis stands have similar greenhouse gas emissions in a New England marsh. Aquat Bot 116:83–92. https://doi.org/10.1016/j.aquabot.2014.01.010

    Article  Google Scholar 

  20. Macreadie PI, Anton A, Raven JA et al (2019) The future of Blue Carbon Science. Nature 10:3998. https://doi.org/10.1038/s41467-019-11693-w

    Article  CAS  Google Scholar 

  21. Chaudhary DR, Kim J, Kang H (2018) Influences of different halophyte vegetation on soil microbial community at temperate salt marsh. Microb Ecol 75:729–738. https://doi.org/10.1007/s00248-017-1083-y

    Article  CAS  PubMed  Google Scholar 

  22. Yuan J, Ding W, Liu D, Kang H, Xiang J, Lin Y (2016) Shifts in methanogen community structure and function across a coastal marsh transect: effects of exotic Spartina alterniflora invasion. Sci Rep 6:18777. https://doi.org/10.1038/srep18777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Yuan J, Liu D, Ji Y, Xiang J, Lin Y, Wu M, Ding W (2019) Spartina alterniflora invasion drastically increases methane production potential by shifting methanogenesis from hydrogenotrophic to methylotrophic pathway in a coastal marsh. J Ecol 107:2436–2450. https://doi.org/10.1111/1365-2745.13164

    Article  CAS  Google Scholar 

  24. Gao G-F, Li P-F, Zhong J-X, Shen Z-J, Chen J, Li Y-T, Isabwe A, Zhu X-Y, Ding Q-S, Zhang S, Gao C-H, Zheng H-L (2019) Spartina alterniflora invasion alters soil bacterial communities and enhances soil N2O emissions by stimulating soil denitrification in mangrove wetland. Sci Total Environ 653:231–240. https://doi.org/10.1016/j.scitotenv.2018.10.277

    Article  CAS  PubMed  Google Scholar 

  25. Wang W, Sardans J, Wang C, Zeng C, Tong C, Chen G, Huang J, Pan H, Peguero G, Vallicrosa H, Peñuelas J (2019) The response of stocks of C, N, and P to plant invasion in the coastal wetlands of China. Glob Chang Biol 25:733–743. https://doi.org/10.1111/gdb.14491

    Article  PubMed  Google Scholar 

  26. Hirano S, Matsumoto N, Morita M, Sasaki K, Ohmura N (2013) Electrochemical control of redox potential affects methanogenesis of the hydrogenotrophic methanogen Methanothermobacter thermautrotrophicus. Lett Appl Microbiol 56:315–321. https://doi.org/10.1111/lam.12059

    Article  CAS  PubMed  Google Scholar 

  27. Kim J, Chaudhary DR, Kang H (2020) Nitrogen addition differently alters GHGs production and soil microbial community of tidal salt marsh soil depending on the types of halophyte. Appl Soil Ecol 150:103440. https://doi.org/10.1016/j.apsoil.2019.103440

    Article  Google Scholar 

  28. Zeleke J, Sheng Q, Wang J-G, Huang M-Y, Xia F, Wu J-H, Quan Z-X (2013) Effects of Spartina alterniflora invasion on the communities of methanogens and sulfate-reducing bacteria in estuarine marsh sediments. Front Microbiol 4:243. https://doi.org/10.3389/fmicb.2013.00243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Sela-Adler M, Ronen Z, Herut B, Antler G, Vigderovich H, Eckert W, Sivan O (2017) Co-existence of methanogenesis and sulfate reduction with common substrates in sulfate-rich estuarine sediments. Front Microbiol 8:766. https://doi.org/10.3389/fmicb.2017.00766

    Article  PubMed  PubMed Central  Google Scholar 

  30. Zaremba-Niedzwiedzka K, Caceres EF, Saw JH et al (2017) Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature 541:353–358. https://doi.org/10.1038/nature21031

    Article  CAS  PubMed  Google Scholar 

  31. Corwin DL, Yemoto K (2020) Salinity: electrical conductivity and total dissolved solids. Soil Sci Soc Am J 84(5):1442–1461. https://doi.org/10.1002/saj2.20154

  32. Bolyen E, Rideout JR, Dillon MR et al (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37:852–857. https://doi.org/10.1038/s41587-019-0209-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583. https://doi.org/10.1038/nmeth.3869

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Price MN, Dehal PS, Arkin AP (2010) FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS ONE 5:e9490. https://doi.org/10.1371/journal.pone.0009490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Bokulich NA, Kaehler BD, Rideout JR, Dillon M, Bolyen E, Knight R, Huttley GA, Caporaso JG (2018) Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin. Microbiome 6:90. https://doi.org/10.1186/s40168-018-0470-z

    Article  PubMed  PubMed Central  Google Scholar 

  37. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596. https://doi.org/10.1093/nar/gks1219

    Article  CAS  PubMed  Google Scholar 

  38. Unite Community (2019) UNITE QIIME release for fungi. Version 18.11.2018. https://forum.qiime2.org/t/unite-v-8-0-2018-11-18-classifiers-for-qiime2-available-here/8750

  39. Rognes T, Flouri T, Nichols B, Quince C, Mahé F (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ 4:e2584. https://doi.org/10.7717/peerj.2584

    Article  PubMed  PubMed Central  Google Scholar 

  40. Barbera P, Kozlov AM, Czech L, Morel B, Darriba D, Flouri T, Stamatakis A (2019) EPA-ng: massively parallel evolutionary placement of genetic sequences. Syst Biol 68:365–369. https://doi.org/10.1093/sysbio/syy054

    Article  PubMed  Google Scholar 

  41. Czech L, Barbera P, Stamatakis A (2020) Genesis and Gappa: processing, analyzing and visualizing phylogenetic (placement) data. Bioinformatics 36(10):3263–3265. https://doi.org/10.1093/bioinformatics/btaa070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Douglas GM, Maffei VJ, Zaneveld J, Yurgel SN, Brown JR, Taylor CM, Huttenhower C, Langille MGI (2020) PICRUSt2: an improved and extensible approach for metagenome inference. bioRxiv 672295. https://doi.org/10.1101/672295

  43. Louca S, Doebeli M (2018) Efficient comparative phylogenetics on large trees. Bioinformatics 34:1053–1055. https://doi.org/10.1093/bioinformatics/btx701

    Article  CAS  PubMed  Google Scholar 

  44. Ye Y, Doak TG (2009) A parsimony approach to biological pathway reconstruction/inference for genomes and metagenomes. PLoS Comput Biol 5:e1000465. https://doi.org/10.1371/journal.pcbi.1000465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Curtis PS, Balduman LM, Drake BG, Whigham DF (1990) Elevated atmospheric CO2 effects on belowground processes in C3 and C4 estuarine marsh communities. Ecology 71:2001–2006. https://doi.org/10.2307/1937608

    Article  Google Scholar 

  46. Berendsen RL, Pieterse CM, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486. https://doi.org/10.1016/j.tplants.2012.04.001

    Article  CAS  PubMed  Google Scholar 

  47. Eilers KG, Lauber CL, Knight R, Fierer N (2010) Shifts in bacterial community structure associated with inputs of low molecular weight carbon compounds to soil. Soil Biol Biochem 42:896–903. https://doi.org/10.1016/j.soilbio.2010.02.003

    Article  CAS  Google Scholar 

  48. Armstrong W, Cousins D, Armstrong J, Turner DW, Beckett PM (2000) Oxygen distribution in wetland plant roots and permeability barriers to gas-exchange with the rhizosphere: a microelectrode and modeling study with Phragmites australis. Ann Bot 86:687–703. https://doi.org/10.1006/anbo.2000.1236

    Article  Google Scholar 

  49. Youssef NH, Rinke C, Stepanauskas R, Farag I, Woyke T, Elshahed MS (2015) Insights into the metabolism, lifestyle and putative evolutionary history of the novel archaeal phylum ‘Diapherotrites.’ ISME J 9:447–460. https://doi.org/10.1038/ismej.2014.141

    Article  CAS  PubMed  Google Scholar 

  50. Kirwan ML, Megonigal JP (2013) Tidal wetland stability in the face of human impacts and sea-level rise. Nature 504:53–60. https://doi.org/10.1038/nature12856

    Article  CAS  PubMed  Google Scholar 

  51. Howes BL, Howarth RW, Teal JM, Valiela I (1981) Oxidation-reduction potentials in a salt marsh: spatial patterns and interactions with primary production. Limnol Oceanogr 26:350–360

    Article  Google Scholar 

  52. Pester M, Schleper C, Wagner M (2011) The Thaumarchaeota: an emerging view of their phylogeny and ecophysiology. Curr Opin Microbiol 14:300–306. https://doi.org/10.1016/j.mib.2011.04.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Liao C, Luo Y, Jiang L, Zhou X, Wu X, Fang C et al (2007) Invasion of Spartina alterniflora enhanced ecosystem carbon and nitrogen stocks in the Yangtze estuary. China Ecosystems 10:1351–1361. https://doi.org/10.1007/s10021-007-9103-2

    Article  CAS  Google Scholar 

  54. Pratscher J, Dumont MG, Conrad R (2011) Ammonia oxidation coupled to CO2 fixation by archaea and bacteria in an agricultural soil. Proc Natl Acad Sci USA 108:4170–4175. https://doi.org/10.1073/pnas.1010981108

    Article  PubMed  PubMed Central  Google Scholar 

  55. Schleper C, Nicol GW (2010) Ammonia-oxidising archaea - physiology, ecology and evolution. Adv Microb Physiol 57:1–41. https://doi.org/10.1016/B978-0-12-381045-8.00001-1

    Article  CAS  PubMed  Google Scholar 

  56. Di HJ, Cameron KC, Shen JP, Winefield CS, O’Callaghan M, Bowatte S, He JZ (2010) Ammonia-oxidizing bacteria and archaea grow under contrasting soil nitrogen conditions. FEMS Microbiol Ecol 72:386–394. https://doi.org/10.1111/j.1574-6941.2010.00861.x

    Article  CAS  PubMed  Google Scholar 

  57. Liu D, Ding W, Jia Z, Cai Z (2012) The impact of dissolved organic carbon on the spatial variability of methanogenic archaea communities in natural wetland ecosystems across China. Appl Microbiol biotechnol 96:253–263. https://doi.org/10.1007/s00253-011-3842-x

    Article  CAS  PubMed  Google Scholar 

  58. Mueller P, Jensen K, Megonigal JP (2016) Plants mediate soil organic matter decomposition in response to sea level rise. Glob Chang Biol 22:404–414. https://doi.org/10.1111/gcb.13082

    Article  PubMed  Google Scholar 

  59. Kuzyakov Y (2010) Priming effects: interactions between living and dead organic matter. Soil Biol Biochem 42:1363–1371. https://doi.org/10.1016/j.soilbio.2010.04.003

    Article  CAS  Google Scholar 

  60. Zhu J-K (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445. https://doi.org/10.1016/S1369-5266(03)00085-2

    Article  CAS  PubMed  Google Scholar 

  61. Cabot C, Sibole JV, Barceló J, Poschenrieder C (2014) Lessons from crop plants struggling with salinity. Plant Sci 226:2–13. https://doi.org/10.1016/j.plantsci.2014.04.013

    Article  CAS  PubMed  Google Scholar 

  62. Ishika T, Hahri PA, Laird DW, Moheimani NR (2018) The effect of gradual increase in salinity on the biomass productivity and biochemical composition of several marine, halotolerant, and halophilic microalgae. J Appl Phycol 30:1453–1464. https://doi.org/10.1007/s10811-017-1377-y

    Article  CAS  Google Scholar 

  63. Schröder M, Sondermann M, Sures B, Hering D (2015) Effects of salinity gradients on benthic invertebrate and diatomcommunities in a German lowland river. Ecol Indic 57:236–248. https://doi.org/10.1016/j.ecolind.2015.04.038

    Article  Google Scholar 

Download references

Acknowledgements

We thank to Laura Simons for the contribution in the English editing of the manuscript.

Funding

The study is supported by the funds from the Ministry of Education of Korea (2019R1A6A3A01091184, 2020R1I1A2072824), the Ministry of Science and ICT of Korea (2018K2A9A1A01090455, 2019K1A3A1A74107424, 2019K1A3A1A80113041), and the Ministry of Oceans and Fisheries of Korea (20170318). Jeongeun Yun was supported by the funds from the Ministry of Education of Korea (NRF-2019H1A2A1076239; Global Ph.D. Fellowship Program).

Author information

Author notes

    Authors and Affiliations

    1. School of Civil and Environmental Engineering, Yonsei University, Seoul, 03722, Republic of Korea

      Jinhyun Kim, Jeongeun Yun & Hojeong Kang

    2. College of Life Sciences & Biotechnology, Korea University, Seoul, 02841, Republic of Korea

      Young Mok Heo, Hanbyul Lee & Jae-Jin Kim

    3. Division of Environmental Science & Ecological Engineering, Korea University, Seoul, 02841, Republic of Korea

      Jae-Jin Kim

    Authors
    1. Jinhyun Kim
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Young Mok Heo
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Jeongeun Yun
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Hanbyul Lee
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Jae-Jin Kim
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Hojeong Kang
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding authors

    Correspondence to Jae-Jin Kim or Hojeong Kang.

    Ethics declarations

    Conflict of Interest

    The authors declare competing interests.

    Additional information

    Jinhyun Kim and Young Mok Heo contributed equally to this work.

    Supplementary Information

    Below is the link to the electronic supplementary material.

    Supplementary file1 (DOCX 27 KB)

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Kim, J., Heo, Y.M., Yun, J. et al. Changes in Archaeal Community and Activity by the Invasion of Spartina anglica Along Soil Depth Profiles of a Coastal Wetland. Microb Ecol 83, 436–446 (2022). https://doi.org/10.1007/s00248-021-01770-3

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s00248-021-01770-3

    Keywords

    Search

    Navigation