Skip to main content

Advertisement

Log in

Influence of the Changjiang River Flood on Synechococcus Ecology in the Surface Waters of the East China Sea

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

Abstract

Synechococcus spp. have been suggested as the primary component of picophytoplankton in the East China Sea (ECS). However, the influences of sudden environmental changes on Synechococcus assemblage composition have not yet been investigated. In the summer of 2010, a disastrous flood occurred in the Changjiang River basin. To improve our understanding of how this flood affected the Synechococcus ecology on the ECS surface, their assemblages and distributions have been described using two-laser flow cytometry and phylogenetic analysis of the phycocyanin operon. During the nonflooding summer of 2009, phycoerythrin-rich (PE-rich) Synechococcus thrived near the outer boundary of the Changjiang River diluted water (CDW) coverage, while phycocyanin-rich (PC-rich) Synechococcus predominated inside the turbid CDW with a transparency of <80 %. During the 2010 summer, flooding expanded the CDW coverage area to over half of the ECS. PE-rich cells showed a homogeneous distribution and a decline in abundance, while the spatial pattern of the PC-rich Synechococcus resembled the pattern from 2009. Based on the phycocyanin operon phylogeny, the Synechococcus in the ECS were categorized into five groups, ECS-1 to ECS-4 and ECS-PE, comprising a total of 19 operational taxonomic units. In the summer of 2009, ECS-2 dominated in the coast, and the ECS-3 and ECS-PE clades prevailed in the offshore waters. However, during the summer of 2010, ECS-4 and ECS-PE became the dominant strains. The injection of abundant anthropogenic pollutants and the enhancement of transparency within the CDW expansion area appear to be the factors needed to transiently alter the ecology of Synechococcus after flooding.

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

Access this article

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  1. Waterbury JB, Watson SW, Guillard RRL, Brand LE (1979) Widespread occurrence of a unicellular, marine, planktonic, cyanobacterium. Nature 277:293–294

    Article  Google Scholar 

  2. Chisholm SW, Olson RJ, Zettler ER, Goericke R, Waterbury JB, Welschmeyer NA (1988) A novel free-living prochlorophyte abundant in the oceanic euphotic zone. Nature 334:340–343

    Article  Google Scholar 

  3. Goericke R, Welschmeyer NA (1993) The marine prochlorophyte Prochlorococcus contributes significantly to phytoplankton biomass and primary production in the Sargasso Sea. Deep Sea Res I 40:2283–2294

    Article  Google Scholar 

  4. Liu H, Campbell L, Landry MR (1995) Growth and mortality rates of Prochlorococcus and Synechococcus measured with a selective inhibitor techniaue. Mar Ecol Prog Ser 116:277–287

    Article  Google Scholar 

  5. Liu H, Nolla HA, Campbell L (1997) Prochlorococcus growth rate and contribution to primary production in the equatorial and subtropical North Pacific Ocean. Aquat Microb Ecol 12:39–47

    Article  Google Scholar 

  6. Richardson TL, Jackson GA (2007) Small phytoplankton and carbon export from the surface ocean. Science 315:838–840

    Article  CAS  PubMed  Google Scholar 

  7. Partensky F, Blanchot J, Vaulot D (1999) Differential distribution and ecology of Prochlorococcus and Synechococcus in oceanic waters: a review. Mar Cyanobacteria 19:457–475

    Google Scholar 

  8. Zwirglmaier K, Jardillier L, Ostrowski M, Mazard S, Garczarek L, Vaulot D, Not F, Massana R, Ulloa O, Scanlan DJ (2008) Global phylogeography of marine Synechococcus and Prochlorococcus reveals a distinct partitioning of lineages among oceanic biomes. Environ Microbiol 10:147–161

    PubMed  Google Scholar 

  9. Chung C-C, Chang J, Gong G-C, Hsu S-C, Chiang K-P, Liao C-W (2011) Effects of Asian dust storms on Synechococcus populations in the subtropical Kuroshio Current. Mar Biotechnol 13:751–763

    Article  CAS  PubMed  Google Scholar 

  10. Herut B, Zohary T, Krom MD, Mantoura RFC, Pitta P, Psarra S, Rassoulzadegan F, Tanaka T, Thingstad TF (2005) Response of East Mediterranean surface water to Saharan dust: on-board microcosm experiment and field observations. Deep Sea Res II 52:3024–3040

    Article  Google Scholar 

  11. Herdman M, Castenholz RW, Iteman I, Waterbury JB, Rippka R (2001) The Archaea and the deeply branching and phototrophic bacteria. In: Boone DR, Castenholz RW (eds) Bergey's manual of systematic bacteriology, vol 1. Springer, Heidelberg, pp 493–514

    Google Scholar 

  12. Scanlan D (2003) Physiological diversity and niche adaptation in marine Synechococcus. Adv Microb Physiol 47:1–64

    Article  CAS  PubMed  Google Scholar 

  13. Waterbury JB, Rippka R (1989) Order Croococcales (Wettstein 1924, emend. Rippka et al. 1979). In: Staley JT, Bryant MP, Pfennig N, Holt JG (eds) Bergey's manual of systematic bacteriology, vol 3. Williams and Wilkins, Baltimore, pp 1728–1739

    Google Scholar 

  14. Stomp M, Huisman J, Vörös L, Pick FR, Laamanen M, Haverkamp T, Stal LJ (2007) Colourful coexistence of red and green picocyanobacteria in lakes and seas. Ecol Lett 10:290–298

    Article  PubMed  Google Scholar 

  15. Six C, Thomas J-C, Garczarek L, Ostrowski M, Dufresne A, Blot N, Scanlan D, Partensky F (2007) Diversity and evolution of phycobilisomes in marine Synechococcus spp.: a comparative genomics study. Genome Biol 8:R259

    Article  PubMed Central  PubMed  Google Scholar 

  16. Jiao N, Yang Y, Hong N, Ma Y, Harada S, Koshikawa H, Watanabe M (2005) Dynamics of autotrophic picoplankton and heterotrophic bacteria in the East China Sea. Cont Shelf Res 25:1265–1279

    Article  Google Scholar 

  17. Liu H, Dagg M, Campbell L, Urban-Rich J (2004) Picophytoplankton and bacterioplankton in the Mississippi River plume and its adjacent waters. Estuaries 27:147–156

    Article  Google Scholar 

  18. Palenik B (2001) Chromatic adaptation in marine Synechococcus strains. Appl Environ Microbiol 67:991–994

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  19. Ferris MJ, Palenik B (1998) Niche adaptation in ocean cyanobacteria. Nature 396:226–228

    Article  CAS  Google Scholar 

  20. Rocap G, Distel DL, Waterbury JB, Chisholm SW (2002) Resolution of Prochlorococcus and Synechococcus ecotypes by using 16S-23S ribosomal DNA internal transcribed spacer sequences. Appl Environ Microbiol 68:1180–1191

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  21. Fuller N, Marie D, Partensky F, Vaulot D, Post A, Scanlan D (2003) Clade-specific 16S ribosomal DNA oligonucleotides reveal the predominance of a single marine Synechococcus clade throughout a stratified water column in the Red Sea. Appl Environ Microbiol 69:2430–2443

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  22. Mühling M, Fuller NJ, Somerfield PJ, Post AF, Wilson WH, Scanlan DJ, Joint I, Mann NH (2006) High resolution genetic diversity studies of marine Synechococcus isolates using rpoC1-based restriction fragment length polymorphism. Aquat Microb Ecol 45:263–275

    Article  Google Scholar 

  23. Chen F, Wang K, Kan J, Bachoon DS, Lu J, Lau S, Campbell L (2004) Phylogenetic diversity of Synechococcus in the Chesapeake Bay revealed by ribulose-1,5-bisphosphate carboxylase-oxygenase (RuBisCO) large subunit gene (rbcL) sequences. Aquat Microb Ecol 36:153–164

    Article  Google Scholar 

  24. Haverkamp T, Acinas S, Doeleman M, Stomp M, Huisman J, Stal L (2008) Diversity and phylogeny of Baltic Sea picocyanobacteria inferred from their ITS and phycobiliprotein operons. Environ Microbiol 10:174–188

    CAS  PubMed  Google Scholar 

  25. Haverkamp THA, Schouten D, Doeleman M, Wollenzien U, Huisman J, Stal LJ (2009) Colorful microdiversity of Synechococcus strains (picocyanobacteria) isolated from the Baltic Sea. ISME J 3:397–408

    Article  CAS  PubMed  Google Scholar 

  26. Gong G-C, Lee Chen Y-L, Liu K-K (1996) Chemical hydrography and chlorophyll a distribution in the East China Sea in summer: implications in nutrient dynamics. Cont Shelf Res 16:1561–1590

    Article  Google Scholar 

  27. Daoji L, Daler D (2004) Ocean pollution from land-based sources: East China Sea, China. AMBIO 33:107–113

    Article  Google Scholar 

  28. Gong GC, Liu KK, Chiang KP, Hsiung TM, Chang J, Chen CC, Hung CC, Chou WC, Chung CC, Chen HY, Shiah FK, Tsai AY, Hsieh C, Shiao JC, Tseng CM, Hsu SC, Lee HJ, Lee MA, Lin II, Tsai F (2011) Yangtze River floods enhance coastal ocean phytoplankton biomass and potential fish production. Geophys Res Lett 38, L13603

    Google Scholar 

  29. Jiao N, Yang Y, Koshikawa H, Watanabe M (2002) Influence of hydrographic conditions on picoplankton distribution in the East China Sea. Aquat Microb Ecol 30:37–48

    Article  Google Scholar 

  30. Chiang K-P, Kuo M-C, Chang J, Wang R-H, Gong G-C (2002) Spatial and temporal variation of the Synechococcus population in the East China Sea and its contribution to phytoplankton biomass. Cont Shelf Res 22:3–13

    Article  Google Scholar 

  31. Gong G-C, Shiah F-K, Liu K-K, Wen Y-H, Liang M-H (2000) Spatial and temporal variation of chlorophyll a, primary productivity and chemical hydrography in the southern East China Sea. Cont Shelf Res 20:411–436

    Article  Google Scholar 

  32. Gong G-C, Wen Y-H, Wang B-W, Liu G-J (2003) Seasonal variation of chlorophyll a concentration, primary production and environmental conditions in the subtropical East China Sea. Deep Sea Res II 50:1219–1236

    Article  CAS  Google Scholar 

  33. Gong G-C, Chang J, Wen Y-H (1999) Estimation of annual primary production in the Kuroshio waters northeast of Taiwan using a photosynthesis-irradiance model. Deep Sea Res I 46:93–108

    Article  Google Scholar 

  34. Lu Y-H, Hwang S-PL, Chen K-M, Chung C-C, Li H-P, Hsiung T-M, Chang J (2001) Isolation and identification of a picophytoplankton, Nannochloris sp., in coastal waters of northern Taiwan. Acta Oceanogr Taiwanica 39:83–92

    CAS  Google Scholar 

  35. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31:3497–3500

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  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 75:7537–7541

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  37. Crosbie ND, Pockl M, Weisse T (2003) Dispersal and phylogenetic diversity of nonmarine picocyanobacteria, inferred from 16S rRNA gene and cpcBA-intergenic spacer sequence analyses. Appl Environ Microbiol 69:5716–5721

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  38. Robertson BR, Tezuka N, Watanabe MM (2001) Phylogenetic analyses of Synechococcus strains (cyanobacteria) using sequences of 16S rDNA and part of the phycocyanin operon reveal multiple evolutionary lines and reflect phycobilin content. Int J Syst Evol Microbiol 51:861–871

    Article  CAS  PubMed  Google Scholar 

  39. Chang J, Lin K-H, Chen K-M, Gong G-C, Chiang K-P (2003) Synechococcus growth and mortality rates in the East China Sea: range of variations and correlation with environmental factors. Deep-Sea Res II 50:1265–1278

    Article  Google Scholar 

  40. Chung C-C, Gong G-C, Hung C-C (2012) Effect of Typhoon Morakot on microphytoplankton population dynamics in the subtropical Northwest Pacific. Mar Ecol Prog Ser 448:39–49

    Article  Google Scholar 

  41. Jiann K-T, Wen L-S, Gong G-C (2009) Distribution and behaviors of Cd, Cu, and Ni in the East China Sea surface water off the Changjiang estuary. Terr Atmos Ocean Sci 20:433–443

    Article  Google Scholar 

  42. Liu JT, Kao S-J, Huh C-A, Hung C-C (2013) Gravity flows associated with flood events and carbon burial: Taiwan as instructional source area. Annu Rev Mar Sci 5:47–68

    Article  CAS  Google Scholar 

  43. Satoh A, Vudikaria LQ, Kurano N, Miyachi S (2005) Evaluation of the sensitivity of marine microalgal strains to the heavy metals, Cu, As, Sb, Pb and Cd. Environ Int 31:713–722

    Article  CAS  PubMed  Google Scholar 

  44. Caroppo C, Stabili L, Aresta M, Corinaldesi C, Danovaro R (2006) Impact of heavy metals and PCBs on marine picoplankton. Environ toxicol 21:541–551

    Article  CAS  PubMed  Google Scholar 

  45. Miao AJ, Wang WX, Juneau P (2009) Comparison of Cd, Cu, and Zn toxic effects on four marine phytoplankton by pulse-amplitude–modulated fluorometry. Environ Toxicol Chem 24:2603–2611

    Article  Google Scholar 

  46. Echeveste P, Dachs J, Berrojalbiz N, Agustí S (2010) Decrease in the abundance and viability of oceanic phytoplankton due to trace levels of complex mixtures of organic pollutants. Chemosphere 81:161–168

    Article  CAS  PubMed  Google Scholar 

  47. Partensky F, Garczarek L (2010) Prochlorococcus: advantages and limits of minimalism. Annu Rev Mar Sci 2:305–331

    Article  Google Scholar 

  48. Partensky F, Hess WR, Vaulot D (1999) Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 63:106–127

    PubMed Central  CAS  PubMed  Google Scholar 

  49. Fuller NJ, Tarran GA, Yallop M, Orcutt KM, Scanlan DJ (2006) Molecular analysis of picocyanobacteria community structure along an Arabian Sea transect reveals distinct spatial separation of lineages. Limnol Oceanogr 51:2515–2526

    Article  Google Scholar 

  50. Stomp M, Huisman J, de Jongh F, Veraart AJ, Gerla D, Rijkeboer M, Ibelings BW, Wollenzien UIA, Stal LJ (2004) Adaptive divergence in pigment composition promotes phytoplankton biodiversity. Nature 432:104–107

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank the captain and crew of the research vessel Ocean Researcher I for their assistance. We are also grateful for the helpful suggestions and comments from the chief editor, Dr. K. E. Nelson, and three anonymous reviewers. This study was supported by the National Science Council of Taiwan (NSC99-2611-M-019-014-MY2 and NSC101-2611-M-019-014) and the Center of Excellence for the Oceans of National Taiwan Ocean University.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chih-Ching Chung.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PPTX 308 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chung, CC., Huang, CY., Gong, GC. et al. Influence of the Changjiang River Flood on Synechococcus Ecology in the Surface Waters of the East China Sea. Microb Ecol 67, 273–285 (2014). https://doi.org/10.1007/s00248-013-0299-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-013-0299-8

Keywords