Skip to main content
SpringerLink
Log in

Structures of bacterial communities on the surface of Ulva prolifera and in seawaters in an Ulva blooming region in Jiaozhou Bay, China

  • Original Paper
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Bacterial community structure on the surface of Ulva prolifera thalli and in seawater in an Ulva blooming region in Jiaozhou Bay was investigated by methods of denaturing gradient gel electrophoresis and 16S rDNA clone libraries. Statistical analysis on the clone libraries indicated that bacterial community structure presented no significant differences between two algal samples. Thallus-surface bacterial communities identified by 16S rDNA clone library were dominated by Alteromonadales, Flavobacteriales, and Rhodobacterales. Sequences affiliated with Gammaproteobacteria, Alphaproteobacteria and CFB were detected in all the four seawater samples. However, their different distribution frequencies among the four samples and the presence of some specific bacterial clusters in some samples indicated changes in the bacterial community composition over the course of the bloom. The dominant bacterial clades changed from Alteromonadales and Rickettsiales in A-SW, to Flavobacteriales and Alteromonadales in B-SW, to Alteromonadales and Campylobacterales in C-SW, and to Rickettsiales, Rhodobacterales and Flavobacteriales in D-SW. Some specific dominant bacterial assemblages were present in some seawater samples, such as Campylobacterales in C-SW and Actinobacteria in D-SW. Our results give an insight into the changes in the bacterial community composition in seawater in blooming region during the course of macroalgal Ulva bloom.

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

Similar content being viewed by others

References

  • Abell G, Bowman J (2005) Ecological and biogeographic relationships of class Flavobacteria in the Southern Ocean. FEMS Microbiol Ecol 51:265–277

    Article  CAS  Google Scholar 

  • Acinas S, Anton J, Rodriguez-Valera F (1999) Diversity of free-living and attached bacteria in offshore western Mediterranean waters as depicted by analysis of genes encoding 16S rRNA. Appl Environ Microbiol 65:514–522

    CAS  Google Scholar 

  • Azam F, Fenchel T, Field J, Gray J, Meyer-Reil L, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263

    Article  Google Scholar 

  • Bird D, Kalff J (1984) Empirical relationships between bacterial abundance and chlorophyll concentration in fresh and marine waters. Can J Fish Aquat Sci 41:1015–1023

    Article  Google Scholar 

  • Blomster J, Back S, Fewer D, Kiirikki M, Lehvo A, Maggs C, Stanhope M (2002) Novel morphology in Enteromorpha (Ulvophyceae) forming green tides. Am J Bot 89:1756–1763

    Article  Google Scholar 

  • Brinkhoff T, Giebel H, Simon M (2008) Diversity, ecology, and genomics of the Roseobacter clade: a short overview. Arch Microbiol 189:531–539

    Article  CAS  Google Scholar 

  • Buchan A, Gonzalez J, Moran M (2005) Overview of the marine Roseobacter lineage. Appl Environ Microbiol 71:5665–5677

    Article  CAS  Google Scholar 

  • Campbell B, Engel A, Porter M, Takai K (2006) The versatile ε-proteobacteria: key players in sulphidic habitats. Nat Rev Microbiol 4:458–468

    Article  CAS  Google Scholar 

  • Cochlan W, Wikner J, Steward G, Smith D, Azam F (1993) Spatial distribution of viruses, bacteria and chlorophyll a in neritic, oceanic and estuarine environments. Mar Ecol Prog Ser 92:77–87

    Article  Google Scholar 

  • Cole J, Findlay S, Pace M (1988) Bacterial production in fresh and saltwater ecosystems: a cross-system overview. Mar Ecol Prog Ser 43:1–10

    Article  Google Scholar 

  • Cottrell M, Waidner L, Yu L, Kirchman D (2005) Bacterial diversity of metagenomic and PCR libraries from the Delaware River. Environ Microbiol 7:1883–1895

    Article  CAS  Google Scholar 

  • Crump B, Hopkinson C, Sogin M, Hobbie J (2004) Microbial biogeography along an estuarine salinity gradient: combined influences of bacterial growth and residence time. Appl Environ Microbiol 70:1494–1505

    Article  CAS  Google Scholar 

  • de Souza MP, Chen YP, Yoch DC (1996) Dimethylsulphoniopropionate lyase from the marine macroalga Ulva curvata: purification and characterisation of the enzyme. Planta 199:433–438

    Article  Google Scholar 

  • DeLong E, Karl D (2005) Genomic perspectives in microbial oceanography. Nature 437:336–342

    Article  CAS  Google Scholar 

  • Dobretsov S, Qian P (2002) Effect of bacteria associated with the green alga Ulva reticulata on marine micro-and macrofouling. Biofouling 18:217–228

    Article  Google Scholar 

  • Fandino L, Riemann L, Steward G, Azam F (2005) Population dynamics of Cytophaga–Flavobacteria during marine phytoplankton blooms analysed by real-time quantitative PCR. Aquat Microb Ecol 40:251–257

    Article  Google Scholar 

  • Feng B, Li X, Wang J, Hu Z, Meng H, Xiang L, Quan Z (2009) Bacterial diversity of water and sediment in the Changjiang estuary and coastal area of the East China Sea. FEMS Microbiol Ecol 70:236–248

    Article  CAS  Google Scholar 

  • Fuse H, Takimura O, Murakami K, Yamaoka Y, Omori T (2000) Utilization of dimethyl sulfide as a sulfur source with the aid of light by Marinobacterium sp. strain DMS-S1. Appl Environ Microbiol 66:5527–5532

    Article  CAS  Google Scholar 

  • Gonzalez J, Simo R, Massana R, Covert J, Casamayor E, Pedros-Alio C, Moran M (2000) Bacterial community structure associated with a dimethylsulfoniopropionate-producing North Atlantic algal bloom. Appl Environ Microbiol 66:4237–4246

    Article  CAS  Google Scholar 

  • Grossart H, Levold F, Allgaier M, Simon M, Brinkhoff T (2005) Marine diatom species harbour distinct bacterial communities. Environ Microbiol 7:860–873

    Article  CAS  Google Scholar 

  • Hewson I, Fuhrman J (2004) Richness and diversity of bacterioplankton species along an estuarine gradient in Moreton Bay, Australia. Appl Environ Microbiol 70:3425–3433

    Article  CAS  Google Scholar 

  • Hirano H, Yoshida T, Fuse H, Endo T, Habe H, Nojiri H, Omori T (2003) Marinobacterium sp. strain DMS-S1 uses dimethyl sulphide as a sulphur source after light-dependent transformation by excreted flavins. Environ Microbiol 5:503–509

    Article  CAS  Google Scholar 

  • Hiraoka M, Ohno M, Kawaguchi S, Yoshida G (2004) Crossing test among floating Ulva thalli forming ‘green tide’ in Japan. Hydrobiologia 512:239–245

    Article  Google Scholar 

  • Kan J, Crump B, Wang K, Chen F (2006) Bacterioplankton community in Chesapeake Bay: predictable or random assemblages. Limnol Oceanogr 51:2157–2169

    Article  CAS  Google Scholar 

  • Kan J, Evans S, Chen F, Suzuki M (2008) Novel estuarine bacterioplankton in rRNA operon libraries from the Chesapeake Bay. Aquat Microb Ecol 51:55–66

    Article  Google Scholar 

  • Kirchman D (2002) The ecology of Cytophaga–Flavobacteria in aquatic environments. FEMS Microbiol Ecol 39:91–100

    CAS  Google Scholar 

  • Ledyard K, DeLong E, Dacey J (1993) Characterization of a DMSP-degrading bacterial isolate from the Sargasso Sea. Arch Microbiol 160:312–318

    Article  CAS  Google Scholar 

  • Lehvo A, Bäck S (2001) Survey of macroalgal mats in the Gulf of Finland, Baltic Sea. Aquat Conserv Mar Freshwat Ecosyst 11:11–18

    Article  Google Scholar 

  • Liu D, Keesing J, Xing Q, Shi P (2009) World’s largest macroalgal bloom caused by expansion of seaweed aquaculture in China. Mar Pollut Bull 58:888–895

    Article  CAS  Google Scholar 

  • Lopez-Garcia P, Duperron S, Philippot P, Foriel J, Susini J, Moreira D (2003) Bacterial diversity in hydrothermal sediment and epsilonproteobacterial dominance in experimental microcolonizers at the Mid-Atlantic Ridge. Environ Microbiol 5:961–976

    Article  CAS  Google Scholar 

  • Lozupone C, Knight R (2007) Global patterns in bacterial diversity. Proc Natl Acad Sci USA 104:11436–11440

    Article  CAS  Google Scholar 

  • Maidak B, Cole J, Lilburn T, Parker C Jr, Saxman P, Farris R, Garrity G, Olsen G, Schmidt T, Tiedje J (2001) The RDP-II (ribosomal database project). Nucleic Acids Res 29:173–174

    Article  CAS  Google Scholar 

  • Martinez J, Smith D, Steward G, Azam F (1996) Variability in ectohydrolytic enzyme activities of pelagic marine bacteria and its significance for substrate processing in the sea. Aquat Microb Ecol 10:223–230

    Article  Google Scholar 

  • Mayali X, Azam F (2004) Algicidal bacteria in the sea and their impact on algal blooms. J Eukaryot Microbiol 51:139–144

    Article  Google Scholar 

  • Mayali X, Franks PJS, Azam F (2008) Cultivation and ecosystem role of a marine Roseobacter clade-affiliated cluster bacterium. Appl Environ Microbiol 74:2595–2603

    Article  CAS  Google Scholar 

  • Morand P, Briand X (1996) Excessive growth of macroalgae: a symptom of environmental disturbance. Bot Mar 39:491–516

    Article  CAS  Google Scholar 

  • Morris RM, Rappé MS, Connon SA, Vergin KL, Siebold WA, Carlson CA, Giovannoni SJ (2002) SAR11 clade dominates ocean surface bacterioplankton communities. Nature 420:806–810

    Article  CAS  Google Scholar 

  • Morris RM, Longnecker K, Giovannoni SJ (2006) Pirellula and OM43 are among the dominant lineages identified in an Oregon coast diatom bloom. Environ Microbiol 8:1361–1370

    Article  CAS  Google Scholar 

  • Muyser G, De Waal E, Uitterlinden A (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700

    Google Scholar 

  • Noble R, Fuhrman J (1997) Virus decay and its causes in coastal waters. Appl Environ Microbiol 63:77–83

    CAS  Google Scholar 

  • Norkko A, Bonsdorff E (2008) Altered benthic prey-availability due to episodic oxygen deficiency caused by drifting algal mats. Mar Ecol 17:355–372

    Article  Google Scholar 

  • Pang S, Liu F, Shan T, Xu N, Zhang Z, Gao S, Chopin T, Sun S (2010) Tracking the algal origin of the Ulva bloom in the Yellow Sea by a combination of molecular, morphological and physiological analyses. Mar Environ Res 69:207–215

    Article  CAS  Google Scholar 

  • Pinhassi J, Sala M, Havskum H, Peters F, Guadayol O, Malits A, Marrase C (2004) Changes in bacterioplankton composition under different phytoplankton regimens. Appl Environ Microbiol 70:6753–6766

    Article  CAS  Google Scholar 

  • Raffaelli D, Raven J, Poole L (1998) Ecological impact of green macroalgal blooms. Oceanogr Mar Biol Annu Rev 36:97–125

    Google Scholar 

  • Rao D, Webb J, Holmstrom C, Case R, Low A, Steinberg P, Kjelleberg S (2007) Low densities of epiphytic bacteria from the marine alga Ulva australis inhibit settlement of fouling organisms. Appl Environ Microbiol 73:7844–7852

    Article  CAS  Google Scholar 

  • Rappé M, Kemp P, Giovannoni S (1997) Phylogenetic diversity of marine coastal picoplankton 16S rRNA genes cloned from the continental shelf off Cape Hatteras, North Carolina. Limnol Oceanogr 42:811–826

    Article  Google Scholar 

  • Riemann L, Steward G, Azam F (2000) Dynamics of bacterial community composition and activity during a mesocosm diatom bloom. Appl Environ Microbiol 66:578–587

    Article  CAS  Google Scholar 

  • Rooney-Varga J, Giewat M, Savin M, Sood S, LeGresley M, Martin J (2005) Links between phytoplankton and bacterial community dynamics in a coastal marine environment. Microb Ecol 49:163–175

    Article  CAS  Google Scholar 

  • Runca E, Bernstein A, Postma L, Di Silvio G (1996) Control of macroalgae blooms in the Lagoon of Venice. Ocean Coast Manage 30:235–257

    Article  Google Scholar 

  • Sapp M, Wichels A, Wiltshire K, Gerdts G (2007) Bacterial community dynamics during the winter–spring transition in the North Sea. FEMS Microbiol Ecol 59:622–637

    Article  CAS  Google Scholar 

  • Schloss P, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71:1501–1506

    Article  CAS  Google Scholar 

  • Selje N, Simon M (2003) Composition and dynamics of particle-associated and free-living bacterial communities in the Weser estuary, Germany. Aquat Microb Ecol 30:221–237

    Article  Google Scholar 

  • Singleton D, Furlong M, Rathbun S, Whitman W (2001) Quantitative comparisons of 16S rRNA gene sequence libraries from environmental samples. Appl Environ Microbiol 67:4374–4376

    Article  CAS  Google Scholar 

  • Skerratt J, Bowman J, Hallegraeff G, James S, Nichols P (2002) Algicidal bacteria associated with blooms of a toxic dinoflagellate in a temperate Australian estuary. Mar Ecol Prog Ser 244:1–15

    Article  Google Scholar 

  • Strom S (2008) Microbial ecology of ocean biogeochemistry: a community perspective. Science 320:1043–1045

    Article  CAS  Google Scholar 

  • Sun C, Zhang M (1998) The measurement of DMSP concentration of microalga and macroalga in part of Jiaozhou Bay. J Ocean Univ Qingdao 28:99–103

    CAS  Google Scholar 

  • Sun S, Wang F, Li C, Qin S, Zhou M, Ding L, Pang S, Duan D, Wang G, Yin B, Yu R, Jiang P, Liu Z, Zhang G, Fei X, Zhou M (2008) Emerging challenges: massive green algae blooms in the Yellow Sea. Nat Preceedings. doi:10101/npre.200802266.200802261

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  Google Scholar 

  • Valiela I, McClelland J, Hauxwell J, Behr P, Hersh D, Foreman K (1997) Macroalgal blooms in shallow estuaries: controls and ecophysiological and ecosystem consequences. Limnol Oceanogr 42:1105–1118

    Article  Google Scholar 

  • Van Alstyne K, Wolfe G, Freidenburg T, Neill A, Hicken C (2001) Activated defense systems in marine macroalgae: evidence for an ecological role for DMSP cleavage. Mar Ecol Prog Ser 213:53–65

    Article  Google Scholar 

  • Wagner-Dobler I, Biebl H (2006) Environmental biology of the marine Roseobacter lineage. Annu Rev Microbiol 60:255–280

    Article  Google Scholar 

  • Weinbauer M, Hornák K, Jezbera J, Nedoma J, Dolan J, Simek K (2007) Synergistic and antagonistic effects of viral lysis and protistan grazing on bacterial biomass, production and diversity. Environ Microbiol 9:777–788

    Article  CAS  Google Scholar 

  • West N, Obernosterer I, Zemb O, Lebaron P (2008) Major differences of bacterial diversity and activity inside and outside of a natural iron-fertilized phytoplankton bloom in the Southern Ocean. Environ Microbiol 10:738–756

    Article  CAS  Google Scholar 

  • Yager P, Connelly T, Mortazavi B, Wommack K, Bano N, Bauer J, Opsahl S, Hollibaugh J (2001) Dynamic bacterial and viral response to an algal bloom at subzero temperatures. Limnol Oceanogr 46:790–801

    Article  CAS  Google Scholar 

  • Zeng J, Yang L, Li J, Liang Y, Xiao L, Jiang L, Zhao D (2009) Vertical distribution of bacterial community structure in the sediments of two eutrophic lakes revealed by denaturing gradient gel electrophoresis (DGGE) and multivariate analysis techniques. World J Microbiol Biotechnol 25:225–233

    Article  CAS  Google Scholar 

  • Zhang R, Liu B, Lau S, Ki J, Qian P (2007) Particle-attached and free-living bacterial communities in a contrasting marine environment: Victoria Harbor, Hong Kong. FEMS Microbiol Ecol 61:496–508

    Article  CAS  Google Scholar 

  • Zubkov M, Fuchs B, Archer S, Kiene R, Amann R, Burkill P (2001) Linking the composition of bacterioplankton to rapid turnover of dissolved dimethylsulphoniopropionate in an algal bloom in the North Sea. Environ Microbiol 3:304–311

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Dr. Ian R. Jenkinson (Agency for Consultation and Research in Oceanography, Lavergne) for language improvement. This study was supported by Project of the Ministry of Science and Technology (2008BAC49B01), and NSFC project 40821004.

Author information

Authors and Affiliations

  1. Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences (CAS), 266071, Qingdao, China

    Min Liu, Yi Dong, Yuan Zhao, Guangtao Zhang, Wuchang Zhang & Tian Xiao

  2. Graduate University of CAS, 100086, Beijing, China

    Min Liu & Yi Dong

  3. Jiaozhou Bay Marine Ecosystem Research Station, CAS, 266071, Qingdao, China

    Guangtao Zhang

Authors
  1. Min Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yi Dong
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yuan Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Guangtao Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wuchang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tian Xiao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tian Xiao.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 753 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, M., Dong, Y., Zhao, Y. et al. Structures of bacterial communities on the surface of Ulva prolifera and in seawaters in an Ulva blooming region in Jiaozhou Bay, China. World J Microbiol Biotechnol 27, 1703–1712 (2011). https://doi.org/10.1007/s11274-010-0627-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11274-010-0627-9

Keywords

Search

Navigation