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Microbial Ecology

, Volume 79, Issue 1, pp 12–20 | Cite as

Seasonal Mixing-Driven System in Estuarine–Coastal Zone Triggers an Ecological Shift in Bacterial Assemblages Involved in Phytoplankton-Derived DMSP Degradation

  • Dukki Han
  • Hee Yoon Kang
  • Chang-Keun Kang
  • Tatsuya Unno
  • Hor-Gil HurEmail author
Microbiology of Aquatic Systems

Abstract

The coastal zone has distinguishable but tightly connected ecosystems from rivers to the ocean and globally contributes to nutrient cycling including phytoplankton-derived organic matter. Particularly, bacterial contributions to phytoplankton-derived dimethylsulfoniopropionate (DMSP) degradation have been recently evaluated by using advanced sequencing technologies to understand their role in the marine microbial food web. Here, we surveyed the bacterial diversity and community composition under seasonal water mixing in the bay of Gwangyang (GW), a semi-enclosed estuary at the southern tip of the Korea Peninsula. We detected phylogenetic dissimilarities among season-specific habitats in GW and their specific bacterial taxa. Additionally, bacterial contribution to degradation of phytoplankton-derived DMSP from estuarine to coastal waters at euphotic depths in GW was investigated as the presence or absence of DMSP demethylation gene, encoded by dmdA. Among the operational taxonomic units (OTUs) in GW bacterial communities, the most dominant and ubiquitous OTU1 was affiliated with the SAR11 clade (SAR11-OTU). The population dynamics of SAR11-OTU in dmdA-detected GW waters suggest that water mass mixing plays a major role in shaping bacterial communities involved in phytoplankton-derived DMSP demethylation.

Keywords

Estuarine–coastal zone Water mass mixing Bacterial biogeography Phylogenetic pattern DMSP dmdA gene 

Notes

Funding information

This study was supported by the project titled “Long-term Marine Ecosystem Research,” funded by the Ministry of Oceans and Fisheries, Korea, and the Basic Science Research Program through the National Research Foundation of Korea funded by the Ministry of Education (NRF-2016R1A6A3A11931896).

Supplementary material

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248_2019_1392_MOESM2_ESM.xlsx (245 kb)
ESM 2 (XLSX 244 kb)
248_2019_1392_MOESM3_ESM.docx (1.2 mb)
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References

  1. 1.
    Chen M, Kim D, Liu H, Kang C-K (2018) Variability in copepod trophic levels and feeding selectivity based on stable isotope analysis in Gwangyang Bay of the southern coast of the Korean Peninsula. Biogeosciences 15:2055–2073Google Scholar
  2. 2.
    Kim D, Baek SH, Yoon D-Y, Kim K-H, Jeong J-H, Jang P-G, Kim Y-O (2014) Water quality assessment at Jinhae Bay and Gwangyang Bay, South Korea. Ocean Sci J 49:251–264Google Scholar
  3. 3.
    Lee JH, Lee D, Kang JJ, Joo HT, Lee JH, Lee HW, Ahn SH, Kang CK, Lee SH (2017) The effects of different environmental factors on the biochemical composition of particulate organic matter in Gwangyang Bay, South Korea. Biogeosciences 14:1903–1917Google Scholar
  4. 4.
    Sul WJ, Oliver TA, Ducklow HW, Amaral-Zettler LA, Sogin ML (2013) Marine bacteria exhibit a bipolar distribution. Proc Natl Acad Sci 110:2342–2347PubMedGoogle Scholar
  5. 5.
    Agogué H, Lamy D, Neal PR, Sogin ML, Herndl GJ (2011) Water mass-specificity of bacterial communities in the North Atlantic revealed by massively parallel sequencing. Mol Ecol 20:258–274PubMedGoogle Scholar
  6. 6.
    Ghiglione J-F, Galand PE, Pommier T, Pedrós-Alió C, Maas EW, Bakker K, Bertilson S, Kirchman DL, Lovejoy C, Yager PL (2012) Pole-to-pole biogeography of surface and deep marine bacterial communities. Proc Natl Acad Sci 109:17633–17638PubMedGoogle Scholar
  7. 7.
    Techtmann SM, Fortney JL, Ayers KA, Joyner DC, Linley TD, Pfiffner SM, Hazen TC (2015) The unique chemistry of eastern Mediterranean water masses selects for distinct microbial communities by depth. PLoS One 10:e0120605PubMedPubMedCentralGoogle Scholar
  8. 8.
    Han D, Ha HK, Hwang CY, Lee BY, Hur H-G, Lee YK (2015) Bacterial communities along stratified water columns at the Chukchi Borderland in the western Arctic Ocean. Deep-Sea Res II Top Stud Oceanogr 120:52–60Google Scholar
  9. 9.
    Han D, Kang I, Ha HK, Kim HC, Kim O-S, Lee BY, Cho J-C, Hur H-G, Lee YK (2014) Bacterial communities of surface mixed layer in the Pacific sector of the western Arctic Ocean during sea-ice melting. PLoS One 9:e86887PubMedPubMedCentralGoogle Scholar
  10. 10.
    Hernando-Morales V, Ameneiro J, Teira E (2017) Water mass mixing shapes bacterial biogeography in a highly hydrodynamic region of the Southern Ocean. Environ Microbiol 19:1017–1029PubMedGoogle Scholar
  11. 11.
    Stegen JC, Fredrickson JK, Wilkins MJ, Konopka AE, Nelson WC, Arntzen EV, Chrisler WB, Chu RK, Danczak RE, Fansler SJ (2016) Groundwater–surface water mixing shifts ecological assembly processes and stimulates organic carbon turnover. Nat Commun 7:11237PubMedPubMedCentralGoogle Scholar
  12. 12.
    Wang J, Shen J, Wu Y, Tu C, Soininen J, Stegen JC, He J, Liu X, Zhang L, Zhang E (2013) Phylogenetic beta diversity in bacterial assemblages across ecosystems: deterministic versus stochastic processes. ISME J 7:1310–1321PubMedPubMedCentralGoogle Scholar
  13. 13.
    Lindemann SR, Moran JJ, Stegen JC, Renslow RS, Hutchison JR, Cole JK, Dohnalkova AC, Tremblay J, Singh K, Malfatti SA (2013) The epsomitic phototrophic microbial mat of Hot Lake, Washington: community structural responses to seasonal cycling. Front Microbiol 4:323PubMedPubMedCentralGoogle Scholar
  14. 14.
    Tripathi BM, Stegen JC, Kim M, Dong K, Adams JM, Lee YK (2018) Soil pH mediates the balance between stochastic and deterministic assembly of bacteria. ISME J 12:1072–1083PubMedPubMedCentralGoogle Scholar
  15. 15.
    Stegen JC, Lin X, Konopka AE, Fredrickson JK (2012) Stochastic and deterministic assembly processes in subsurface microbial communities. ISME J 6:1653–1664PubMedPubMedCentralGoogle Scholar
  16. 16.
    Dini-Andreote F, Stegen JC, van Elsas JD, Salles JF (2015) Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession. Proc Natl Acad Sci:201414261 112:E1326–E1332PubMedGoogle Scholar
  17. 17.
    Amaral-Zettler LA, Zettler ER, Theroux SM, Palacios C, Aguilera A, Amils R (2011) Microbial community structure across the tree of life in the extreme Rio Tinto. ISME J 5:42–50PubMedGoogle Scholar
  18. 18.
    Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505Google Scholar
  19. 19.
    Johnston AW (2015) Who can cleave DMSP? Science 348:1430–1431PubMedGoogle Scholar
  20. 20.
    Levine NM, Varaljay VA, Toole DA, Dacey JW, Doney SC, Moran MA (2012) Environmental, biochemical and genetic drivers of DMSP degradation and DMS production in the Sargasso Sea. Environ Microbiol 14:1210–1223PubMedGoogle Scholar
  21. 21.
    Mou X, Sun S, Edwards RA, Hodson RE, Moran MA (2008) Bacterial carbon processing by generalist species in the coastal ocean. Nature 451:708–711PubMedGoogle Scholar
  22. 22.
    Howard EC, Henriksen JR, Buchan A, Reisch CR, Bürgmann H, Welsh R, Ye W, González JM, Mace K, Joye SB (2006) Bacterial taxa that limit sulfur flux from the ocean. Science 314:649–652PubMedGoogle Scholar
  23. 23.
    Kiene RP, Linn LJ, González J, Moran MA, Bruton JA (1999) Dimethylsulfoniopropionate and methanethiol are important precursors of methionine and protein-sulfur in marine bacterioplankton. Appl Environ Microbiol 65:4549–4558PubMedPubMedCentralGoogle Scholar
  24. 24.
    Varaljay VA, Robidart J, Preston CM, Gifford SM, Durham BP, Burns AS, Ryan JP, Marin III R, Kiene RP, Zehr JP (2015) Single-taxon field measurements of bacterial gene regulation controlling DMSP fate. ISME J 9:1677–1686PubMedPubMedCentralGoogle Scholar
  25. 25.
    Van Duyl FC, Gieskes WW, Kop AJ, Lewis WE (1998) Biological control of short-term variations in the concentration of DMSP and DMS during a Phaeocystis spring bloom. J Sea Res 40:221–231Google Scholar
  26. 26.
    Ledyard KM, Dacey JW (1996) Microbial cycling of DMSP and DMS in coastalandoligotrophicseawater. Limnol Oceanogr 41:33–40Google Scholar
  27. 27.
    Andreae MO, Crutzen PJ (1997) Atmospheric aerosols: biogeochemical sources and role in atmospheric chemistry. Science 276:1052–1058Google Scholar
  28. 28.
    Lovelock JE, Maggs R, Rasmussen R (1972) Atmospheric dimethyl sulphide and the natural sulphur cycle. Nature 237:452–453Google Scholar
  29. 29.
    Simó R (2001) Production of atmospheric sulfur by oceanic plankton: biogeochemical, ecological and evolutionary links. Trends Ecol Evol 16:287–294PubMedGoogle Scholar
  30. 30.
    Howard EC, Sun S, Biers EJ, Moran MA (2008) Abundant and diverse bacteria involved in DMSP degradation in marine surface waters. Environ Microbiol 10:2397–2410PubMedGoogle Scholar
  31. 31.
    Howard EC, Sun S, Reisch CR, del Valle DA, Bürgmann H, Kiene RP, Moran MA (2011) Changes in dimethylsulfoniopropionate demethylase gene assemblages in response to an induced phytoplankton bloom. Appl Environ Microbiol 77:524–531PubMedGoogle Scholar
  32. 32.
    Varaljay VA, Howard EC, Sun S, Moran MA (2010) Deep sequencing of a dimethylsulfoniopropionate-degrading gene (dmdA) by using PCR primer pairs designed on the basis of marine metagenomic data. Appl Environ Microbiol 76:609–617PubMedGoogle Scholar
  33. 33.
    Morris RM, Rappé MS, Connon SA, Vergin KL, Siebold WA, Carlson CA, Giovannoni SJ (2002) SAR11 clade dominates ocean surface bacterioplankton communities. Nature 420:806–810PubMedGoogle Scholar
  34. 34.
    Rusch DB, Halpern AL, Sutton G, Heidelberg KB, Williamson S, Yooseph S, Wu D, Eisen JA, Hoffman JM, Remington K (2007) The Sorcerer II global ocean sampling expedition: Northwest Atlantic through eastern tropical Pacific. PLoS Biol 5:e77PubMedPubMedCentralGoogle Scholar
  35. 35.
    Kwak JH, Lee SH, Hwang J, Suh YS, Park H, Chang KI, Kim KR, Kang CK (2014) Summer primary productivity and phytoplankton community composition driven by different hydrographic structures in the East/Japan Sea and the Western Subarctic Pacific. J Geophys Res Oceans 119:4505–4519Google Scholar
  36. 36.
    Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541PubMedPubMedCentralGoogle Scholar
  37. 37.
    Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Applied and environmental microbiology: AEM. 01043-01013PubMedPubMedCentralGoogle Scholar
  38. 38.
    R Core Team (2013) R: A language and environment for statistical computingGoogle Scholar
  39. 39.
    Oksanen J, Blanchet FG Package ‘vegan’Google Scholar
  40. 40.
    Webb CO, Ackerly DD, Kembel SW (2008) Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 24:2098–2100PubMedGoogle Scholar
  41. 41.
    Roberts DW, Roberts MDW (2016) Package ‘labdsv’Google Scholar
  42. 42.
    Heiberger R (2004) R package’HH’(version 2.2–17). Support software for statistical analysis and data display by Heiberger and HollandGoogle Scholar
  43. 43.
    Hothorn T, Hornik K, Strobl C, Zeileis A, Hothorn MT (2015) Package ‘party’Google Scholar
  44. 44.
    Rappé MS, Connon SA, Vergin KL, Giovannoni SJ (2002) Cultivation of the ubiquitous SAR11 marine bacterioplankton clade. Nature 418:630–633PubMedGoogle Scholar
  45. 45.
    Giebel H-A, Kalhoefer D, Gahl-Janssen R, Choo Y-J, Lee K, Cho J-C, Tindall BJ, Rhiel E, Beardsley C, Aydogmus ÖO (2013) Planktomarina temperata gen. Nov., sp. nov., belonging to the globally distributed RCA cluster of the marine Roseobacter clade, isolated from the German Wadden Sea. Int J Syst Evol Microbiol 63:4207–4217PubMedGoogle Scholar
  46. 46.
    Devictor V, Julliard R, Jiguet F (2008) Distribution of specialist and generalist species along spatial gradients of habitat disturbance and fragmentation. Oikos 117:507–514Google Scholar
  47. 47.
    Chesson P (2000) Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst 31:343–366Google Scholar
  48. 48.
    Fargione J, Brown CS, Tilman D (2003) Community assembly and invasion: an experimental test of neutral versus niche processes. Proc Natl Acad Sci 100:8916–8920PubMedGoogle Scholar
  49. 49.
    Stefels J (2000) Physiological aspects of the production and conversion of DMSP in marine algae and higher plants. J Sea Res 43:183–197Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Dukki Han
    • 1
  • Hee Yoon Kang
    • 2
  • Chang-Keun Kang
    • 2
  • Tatsuya Unno
    • 1
  • Hor-Gil Hur
    • 2
    Email author
  1. 1.Jeju National UniversityJejuRepublic of Korea
  2. 2.School of Earth Sciences and Environmental EngineeringGwangju Institute of Science and TechnologyGwangjuRepublic of Korea

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