Advertisement

Microbial Ecology

, Volume 75, Issue 1, pp 10–21 | Cite as

Variation of Synechococcus Pigment Genetic Diversity Along Two Turbidity Gradients in the China Seas

  • Xiaomin Xia
  • Hongbin Liu
  • Donghan Choi
  • Jae Hoon Noh
Microbiology of Aquatic Systems

Abstract

Synechococcus are important and widely distributed picocyanobacteria that encompass a high pigment diversity. In this study, we developed a primer set (peBF/peAR) for amplifying the cpeBA operon sequence from Synechococcus genomic DNA to study Synechococcus pigment diversity along two turbidity gradients in the China seas. Our data revealed that all previously reported pigment types occurred in the South (SCS) and East (ECS) China Seas. In addition, a novel pigment genetic type (type 3f), represented by the high phycourobilin Synechococcus sp. strain KORDI-100 (Exc495:545 = 2.35), was detected. This pigment genetic type differs from the 3c/3d types not only for a very high PUB/PEB ratio but also for a different intergenic spacer sequence and gene organization of the phycobilisome. Synechococcus of different pigment types exhibited clear niche differentiation. Type 2 dominated in the coastal waters, whereas type 3c/3d and 3f were predominant in oceanic waters of the SCS in summer. In the ECS, however, type 3a was the major pigment type throughout the transect. We suggest that in marine environment, various pigment types often co-occur but with one type dominant and PUB/PEB ratio is related to geographic distribution of Synechococcus pigment types. The two marginal seas of China have markedly different Synechococcus pigment compositions.

Keywords

cpeBA operon China seas Synechococcus pigment type Clone library 

Notes

Acknowledgments

We acknowledge the support of the following research grants: General Research Fund (661912, 661813) by Hong Kong Research Grants Council, the National Key Scientific Research Projects of China (2015CB954003), and Natural Science Foundation of China (41330961). We thank Candy Lee for providing Synechococcus strains.

Supplementary material

248_2017_1021_MOESM1_ESM.docx (1.6 mb)
Fig S1 (DOCX 1626 kb).
248_2017_1021_MOESM2_ESM.docx (1.2 mb)
Fig S2 (DOCX 1219 kb).
248_2017_1021_MOESM3_ESM.docx (305 kb)
Fig S3 (DOCX 304 kb).
248_2017_1021_MOESM4_ESM.docx (2.3 mb)
Fig S4 (DOCX 2335 kb).
248_2017_1021_MOESM5_ESM.docx (79 kb)
Fig S5 (DOCX 78 kb).
248_2017_1021_MOESM6_ESM.docx (40 kb)
Fig S6 (DOCX 39 kb).

References

  1. 1.
    Flombaum P, Gallegos JL, Gordillo RA, Rincón J, Zabala LL, Jiao N, Karl DM, Li WK, Lomas MW, Veneziano D (2013) Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus PNAS 110(24):9824–9829CrossRefPubMedGoogle Scholar
  2. 2.
    Six C, Thomas J-C, Garczarek L, Ostrowski M, Dufresne A, Blot N, Scanlan DJ, Partensky F (2007) Diversity and evolution of phycobilisomes in marine Synechococcus spp.: a comparative genomics study Genome Biol. 8(12):1CrossRefGoogle Scholar
  3. 3.
    Wood M, Horan P, Muirhead K, Phinney D, Yentsch C, Waterbury J (1985) Discrimination between types of pigments in marine Synechococcus spp. by scanning spectroscopy, epifluorescence microscopy, and flow cytometry Limnol. Oceanogr. 30(6):1303–1315CrossRefGoogle Scholar
  4. 4.
    Vörös L, Callieri C, Katalin V, Bertoni R (1998) Freshwater picocyanobacteria along a trophic gradient and light quality range. In: Phytoplankton and trophic gradients. Springer, Netherlands, pp 117–125Google Scholar
  5. 5.
    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(4):290–298CrossRefPubMedGoogle Scholar
  6. 6.
    Everroad C, Six C, Partensky F, Thomas J-C, Holtzendorff J, Wood AM (2006) Biochemical bases of type IV chromatic adaptation in marine Synechococcus spp J. Bacteriol. 188(9):3345–3356CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Scanlan DJ (2012) Marine picocyanobacteria. In: Ecology of Cyanobacteria II. Springer, Berlin pp 503–533Google Scholar
  8. 8.
    Callieri C, Cronberg G, Stockner JG (2012) Freshwater picocyanobacteria: single cells, microcolonies and colonial forms. In: Ecology of Cyanobacteria II. Springer, New York pp 229–269Google Scholar
  9. 9.
    Stomp M, Huisman J, De Jongh F, Veraart AJ, Gerla D, Rijkeboer M, Ibelings BW, Wollenzien UI, Stal LJ (2004) Adaptive divergence in pigment composition promotes phytoplankton biodiversity Nature 432(7013):104–107CrossRefPubMedGoogle Scholar
  10. 10.
    Callieri C (1996) Extinction coefficient of red, green and blue light and its influence on picocyanobacterial types in lakes at different trophic levels Memorie-Istituto Italiano Di Idrobiologia Dott Marco De Marchi 54:135–142Google Scholar
  11. 11.
    Pittera J, Humily F, Thorel M, Grulois D, Garczarek L, Six C (2014) Connecting thermal physiology and latitudinal niche partitioning in marine Synechococcus The ISME Journal 8(6):1221–1236CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Moore LR, Goericke R, Chisholm SW (1995) Comparative physiology of Synechococcus and Prochlorococcus: influence of light and temperature on growth, pigments, fluorescence and absorptive properties Mar. Ecol. Prog. Ser. 116:259–275CrossRefGoogle Scholar
  13. 13.
    Liu H, Jing H, Wong TH, Chen B (2014) Co-occurrence of phycocyanin- and phycoerythrin-rich Synechococcus in subtropical estuarine and coastal waters of Hong Kong Environ. Microbiol. Rep. 6(1):90–99CrossRefPubMedGoogle Scholar
  14. 14.
    Everroad C, Wood M (2006) Comparative molecular evolution of newly discovered picocyanobacterial strains reveals a phylogenetically informative variable region of β-phycoerythrin J. Phycol. 42(6):1300–1311CrossRefGoogle Scholar
  15. 15.
    Everroad C, Wood M (2012) Phycoerythrin evolution and diversification of spectral phenotype in marine Synechococcus and related picocyanobacteria Mol Phylogen Evol 64(3):381–392CrossRefGoogle Scholar
  16. 16.
    Humily F, Partensky F, Six C, Farrant GK, Ratin M, Marie D, Garczarek L (2013) A gene island with two possible configurations is involved in chromatic acclimation in marine Synechococcus PLoS One 8(12):e84459CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Haverkamp T, Acinas SG, Doeleman M, Stomp M, Huisman J, Stal LJ (2008) Diversity and phylogeny of Baltic Sea picocyanobacteria inferred from their ITS and phycobiliprotein operons Environ. Microbiol. 10(1):174–188PubMedGoogle Scholar
  18. 18.
    Xia X, Partensky F, Garczarek L, Suzuki K, Guo C, Cheung SY, Liu H (2016) Phylogeography and pigment type diversity of Synechococcus cyanobacteria in surface waters of the northwestern Pacific Ocean Environ. Microbiol. doi: 10.1111/1462-2920.13541
  19. 19.
    Larsson J, Celepli N, Ininbergs K, Dupont CL, Yooseph S, Bergman B, Ekman M (2014) Picocyanobacteria containing a novel pigment gene cluster dominate the brackish water Baltic Sea The ISME Journal 8(9):1892–1903CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Chung C-C, Huang C-Y, Gong G-C, Lin Y-C (2014) Influence of the Changjiang River flood on Synechococcus ecology in the surface waters of the East China Sea Microb. Ecol. 67(2):273–285CrossRefPubMedGoogle Scholar
  21. 21.
    Xia X, Vidyarathna NK, Palenik B, Lee P, Liu H (2015) Comparison of the seasonal variations of Synechococcus assemblage structures in estuarine waters and coastal waters of Hong Kong Appl. Environ. Microbiol. 81(21):7644–7655CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Liu H, Campbell L, Landry MR, Nolla HA, Brown SL, Constantinou J (1998) Prochlorococcus and Synechococcus growth rates and contributions to production in the Arabian Sea during the 1995 southwest and northeast monsoons Deep Sea Res (II Top Stud Oceanogr) 45(10):2327–2352CrossRefGoogle Scholar
  23. 23.
    Fuller NJ, Marie D, Partensky F, Vaulot D, Post AF, Scanlan DJ (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(5):2430–2443CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Nucleic Acids Res. 22(22):4673–4680CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ (2009) Introducing Mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities Appl. Environ. Microbiol. 75(23):7537–7541CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection Bioinformatics 27(16):2194–2200CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Kumar S, Tamura K, Nei M (1994) MEGA: molecular evolutionary genetics analysis software for microcomputers Computer Applications in the Biosciences: CABIOS 10(2):189–191PubMedGoogle Scholar
  28. 28.
    Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution Bioinformatics 14(9):817–818CrossRefPubMedGoogle Scholar
  29. 29.
    Clarke K, Warwick R (1994) An approach to statistical analysis and interpretation. Change in Marine Communities 2Google Scholar
  30. 30.
    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(3):263–275CrossRefGoogle Scholar
  31. 31.
    Hall TA 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. In: Nucleic acids symposium series, vol 41. [London]. Information Retrieval Ltd., c1979-c2000., pp 95–98Google Scholar
  32. 32.
    Choi DH, Hn J (2009) Phylogenetic diversity of Synechococcus strains isolated from the East China Sea and the East Sea FEMS Microbiol. Ecol. 69(3):439–448CrossRefPubMedGoogle Scholar
  33. 33.
    Olson R, Chisholm S, Zettler E, Armbrust E (1988) Analysis of Synechococcus pigment types in the sea using single and dual beam flow cytometry Deep Sea Res (I Oceanogr Res Pap) 35(3):425–440CrossRefGoogle Scholar
  34. 34.
    Allawi HT, SantaLucia J (1997) Thermodynamics and NMR of internal G-T mismatches in DNA Biochemistry 36(34):10581–10594CrossRefPubMedGoogle Scholar
  35. 35.
    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(1):147–161PubMedGoogle Scholar
  36. 36.
    Choi DH, Noh JH, Lee J-H (2014) Application of pyrosequencing method for investigating the diversity of Synechococcus subcluster 5.1 in open ocean Microbes Environ. 29(1):17CrossRefPubMedGoogle Scholar
  37. 37.
    Lee SK, Wang H, Law SH, Wu RS, Kong RY (2002) Analysis of the 16S–23S rDNA intergenic spacers (IGSs) of marine vibrios for species-specific signature DNA sequences Mar. Pollut. Bull. 44(5):412–420CrossRefPubMedGoogle Scholar
  38. 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(3):861–871CrossRefPubMedGoogle Scholar
  39. 39.
    Haverkamp T, Schouten D, Doeleman M, Wollenzien U, Huisman J, Stal LJ (2009) Colorful microdiversity of Synechococcus strains (picocyanobacteria) isolated from the Baltic Sea The ISME Journal 3(4):397–408CrossRefPubMedGoogle Scholar
  40. 40.
    Kirk JT (1994) Light and photosynthesis in aquatic ecosystems. Cambridge University Press, Cambridge, CrossRefGoogle Scholar
  41. 41.
    Jing H, Zhang R, Pointing SB, Liu H, Qian P (2009) Genetic diversity and temporal variation of the marine Synechococcus community in the subtropical coastal waters of Hong Kong Can. J. Microbiol. 55(3):311–318CrossRefPubMedGoogle Scholar
  42. 42.
    Humily F, Farrant GK, Marie D, Partensky F, Mazard S, Perennou M, Labadie K, Aury J-M, Wincker P, Segui AN (2014) Development of a targeted metagenomic approach to study a genomic region involved in light harvesting in marine Synechococcus FEMS Microbiol. Ecol. 88(2):231–249CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  1. 1.Division of Life ScienceThe Hong Kong University of Science and TechnologyHong KongPeople’s Republic of China
  2. 2.Marine Ecosystem and Biological Research CenterKorea Institute of Ocean Science and TechnologyAnsanRepublic of Korea

Personalised recommendations