Skip to main content

Advertisement

Log in

Phenotype changes of cyanobacterial and microbial distribution characteristics of surface sediments in different periods of cyanobacterial blooms in Taihu Lake

  • Published:
Aquatic Ecology Aims and scope Submit manuscript

Abstract

This study investigates the morphological changes in cyanobacterial and microbial distribution characteristics of surface sediments, throughout different cyanobacterial blooms periods in Zhushan Bay, Taihu Lake. Comparative microscopic analysis of cyanobacterial morphology (n = 36) was performed during the formation period (W1), stationary period (W2), decline period (W3) and decomposition period (W4). Simultaneously, sequence analysis was performed on microbial 16S rRNA genes in sediments (n = 36) by high-throughput sequencing. The coverage of the sequencing library was very high (100%) indicating that the sequencing results well represented the microbes present in samples, among which the species richness in W4 was the highest, while the species distribution uniformity was low. The microbial abundance distribution in all four periods showed that Firmicutes (33.45%), Cyanobacteria (30.44%), Proteobacteria (27.17%) and Bacteroidetes (7.2%) were the dominant flora, with W1 dominated by Cyanobacteria, W2 dominated by Firmicutes, W3 dominated by Proteobacteria and Cyanobacteria, and W4 dominated by Proteobacteria. There were significant differences in microbial species abundance and distribution observed during each cyanobacterial bloom period and synchronous microorganisms in the sediment regulated bacterial abundance and distribution through signal transduction of various proteases. The findings of this study help to establish the impact of cyanobacteria blooms on the sediment environment and benefit the comprehensive assessment of hazard presented by cyanobacteria to the aquatic environment.

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

Access this article

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
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Amato KR, Yeoman CJ, Kent A, Righini N, Carbonero F, Estrada A et al (2013) Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes. ISME J 7:1344–1353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aurélie C, Thierry B, Josette G (2003) Nitrification and nitrifying bacteria in the lower Seine River and estuary (France). App Environ Microbiol 69:70–91

    Google Scholar 

  • Boon AR, Duineveld GCA (1998) Relationships between benthic activity and the annual phytopigment cycle in near-bottom water and sediments in the southern North Sea. Estuar Coast Shelf Sci 46:1–13

    Article  Google Scholar 

  • Bridgeman TB, Chaffin JD, Filbrun JE (2013) A novel method for tracking western lake erie microcystis blooms, 2002–2011. J Great Lakes Res 39(1):83–89

    Article  Google Scholar 

  • Brookes JD, Carey CC (2011) Resilience to blooms. Science 334:46–47

    Article  CAS  PubMed  Google Scholar 

  • Bui HM, Pham LT, Dao ST (2017) Prediction of cyanobacterial blooms in the Dau Tieng reservoir using artificial neural network. Mar Freshw Res 68(11):2070–2080

    Article  CAS  Google Scholar 

  • Cameron KA, Hodson AJ, Mark Osborn A (2012) Structure and diversity of bacterial, eukaryotic and archaeal communities in glacial cryoconite holes from the arctic and the antarctic. FEMS Microbiol Ecol 82(2):254–267

    Article  CAS  PubMed  Google Scholar 

  • Cao X, Wang Y, He J, Luo X, Zheng Z (2016) Phosphorus mobility among sediments, water and cyanobacteria enhanced by cyanobacteria blooms in eutrophic Lake Dianchi. Environ Pollut 219:580

    Article  CAS  PubMed  Google Scholar 

  • Carni SA, Joye SB (2008) Nitrification in Mono Lake, California: activity and community composition during contrasting hydrological regimes. Limnol Oceanogr 53:2546–2557

    Article  Google Scholar 

  • Cebron A, Berthe T, Garnier J (2003) Nitrification and nitrifying bacteria in the lower Seine River and estuary (France). Appl Environ Microbiol 69:7091–7100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Y, Qin B, Teubner K, Dokulil MT (2003) Long-term dynamics of phytoplankton assemblages: microcystis-domination in Lake Taihu, a large shallow lake in China. J Plankton Res 25:445–453

    Article  Google Scholar 

  • Chen GY, Qiu SL, Zhou YY (2009) Diversity and abundance of ammonia-oxidizing bacteria in eutrophic and oligotrophic basins of a shallow Chinese lake (Lake Donghu). Res Microbiol 160:173–178

    Article  CAS  PubMed  Google Scholar 

  • Chuai X, Wei D, Chen X, Wang X, Miao A, Xi B, He L, Yang L (2011) Phosphorus release from cyanobacterial blooms in Meiliang Bay of Lake Taihu, China. Ecol Eng 37:842–849

    Article  Google Scholar 

  • Cumpson PJ, Sano N, Fletcher IW, Portoles JF, Bravo Sanchez M, Barlow AJ (2015) Multivariate analysis of extremely large ToFSIMS imaging datasets by a rapid PCA method. Surf Interface Anal 47:986–993

    Article  CAS  Google Scholar 

  • Dai Y, Yang Y, Wu Z, Feng Q, Xie S, Liu Y (2016) Spatiotemporal variation of planktonic and sediment bacterial assemblages in two plateau freshwater lakes at different trophic status. Appl Microbiol Biotechnol 100:4161–4175

    Article  CAS  PubMed  Google Scholar 

  • De CD, Yokokawa T, Varela MM, Agogué H, Herndl GJ (2015) Spatial distribution of Bacteria and Archaea and amo A gene copy numbers throughout the water column of the Eastern Mediterranean Sea. ISME J 3:147

    CAS  Google Scholar 

  • Deng DG, Xie P, Zhou Q, Yang H, Guo LG (2010) Studies on temporal and spatial variations of phytoplankton in Lake Chaohu. J Integr Plant Biol 49(409):418

    Google Scholar 

  • Denis L, Grenz C, Alliot É, Rodier M (2001) Temporal variability in dissolved inorganic nitrogen fluxes at the sediment–water interface and related annual budget on a continental shelf (NW Mediterranean). Oceanol Acta 24(85):97

    Google Scholar 

  • Downes MT (1988) Aquatic nitrogen transformations at low oxygen concentrations. Appl Environ Microbiol 54:172–175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fay P (1965) Heterotrophy and nitrogen fixation in chlorogloea fritschii. J Gen Microbiol 39(1):11–20

    Article  CAS  PubMed  Google Scholar 

  • Gao G, Yang LY (2008) Physiological and ecological characteristics of bluegreen algae in Lake Taihu. In: Qin B (ed) Lake Taihu, China. Monographiae biologicae, vol 87. Springer, Dordrecht, pp 197–227

    Chapter  Google Scholar 

  • Gómez-Acata S, Esquivel-Ríos I, Pérez-Sandoval MV, Navarro-Noya Y, Dendooven L (2017) Bacterial community structure within an activated sludge reactor added with phenolic compounds. Appl Microbiol Biotechnol 101(8):1–10

    Article  CAS  Google Scholar 

  • Graf G, Bengtsson W, Diesner U, Schulz R, Theede H (1982) Benthic response to sedimentation of a spring phytoplankton bloom: process and budget. Mar Biol 67:201–208

    Article  Google Scholar 

  • Grenzll C, Hager SW, Cole BE (2000) Dynamics of nutrient cycling and related benthic nutrient and oxygen fluxes during a spring phyto-plankton bloom in South San Francisco Bay (USA). Mar Ecol Prog 197:67–80

    Article  Google Scholar 

  • Hallez R, Delaby M, Sanselicio S, Viollier PH (2017) Hit the right spots: cell cycle control by phosphorylated guanosines in alphaproteobacteria. Nat Rev Microbiol 15:137–148

    Article  CAS  PubMed  Google Scholar 

  • Hansen LS, Blackburn TH (1992) Effect of algal bloom deposition on sediment respiration and fluxes. Mar Biol 112:147–152

    Article  Google Scholar 

  • Heike S, Matthias S, Meinhard S, Thorsten B (2010) Phylogeny of proteobacteria and bacteroidetes from oxic habitats of a tidal flat ecosystem. FEMS Microbiol Ecol 54:351–365

    Google Scholar 

  • Huang J, Graham N, Templeton MR, Zhang Y, Collins C, Nieuwenhuijsen M (2009) A comparison of the role of two blue-green algae in THM and HAA formation. Water Res 43:3009–3018

    Article  CAS  PubMed  Google Scholar 

  • Jiao HB, Zha Y, Gao J, Li YM, Wei YC, Huang JZ (2006) Estimation of chlorophyll-a concentration in Lake Tai, China using in situ hyperspectral data. Int J Remote Sens 27:4267–4276

    Article  Google Scholar 

  • Keqiang S, Guang G, Boqiang Q, Xiangming T, Yongping W, Kexu C, Jiangyu D (2011) Comparing sediment bacterial communities in the macrophyte-dominated and algae-dominated areas of eutrophic Lake Taihu, China. Can J Microbiol 57:263–272

    Article  Google Scholar 

  • Khangembam CD, Sharma JG, Chakrabarti R (2018) Diversity and abundance of ammonia-oxidizing bacteria and archaea in a freshwater recirculating aquaculture system. HAYATI J Biosci 24:215–220

    Article  Google Scholar 

  • Köberl M, Dita M, Martinuz A, Staver C, Berg G (2017) Members of gammaproteobacteria as indicator species of healthy banana plants on fusarium wilt-infested fields in central America. Sci Rep 7:45318

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Koho KA, Langezaal AM, Lith YAV, Duijnstee IAP, Zwaan GJVD (2008) The influence of a simulated diatom bloom on deep-sea benthic foraminifera and the activity of bacteria: a mesocosm study. Deep Sea Res Part I 55:696–719

    Article  Google Scholar 

  • Komárek J (2016) Review of the cyanobacterial genera implying planktic species after recent taxonomic revisions according to polyphasic methods: state as of 2014. Hydrobiologia 764(1):259–270

    Article  Google Scholar 

  • León KBD, Utturkar SM, Camilleri LB, Elias DA, Arkin AP, Fields MW et al (2015) Complete genome sequence of Pelosinus fermentans JBW45, a member of a remarkably competitive group of Negativicutes in the Firmicutes phylum. Genome Announc 3(5):e01090-15

    Article  PubMed  PubMed Central  Google Scholar 

  • Li H, Xing P, Chen M, Bian Y, Wu QL (2011) Short-term bacterial community composition dynamics in response to accumulation and breakdown of microcystis blooms. Water Res 45:1702–1710

    Article  CAS  PubMed  Google Scholar 

  • Li H, Xing P, Wu QL (2012) Characterization of the bacterial community composition in a hypoxic zone induced by microcystis blooms in lake Taihu, china. FEMS Microbiol Ecol 79(3):773–784

    Article  CAS  PubMed  Google Scholar 

  • Li J, Yang X, Wang Z, Shan Y, Zheng Z (2015a) Comparison of four aquatic plant treatment systems for nutrient removal from eutrophied water. Bioresource Technol 179:1–7

    Article  CAS  Google Scholar 

  • Li J, Zhang J, Liu L, Fan Y, Li L, Yang Y et al (2015b) Annual periodicity in planktonic bacterial and archaeal community composition of eutrophic lake Taihu. Sci Rep 5:15488

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li CY, Hu H, Feng JY, Mbadinga SM, Liu JF, Yang SZ et al (2016) Diversity and abundance of ammonia-oxidizing bacteria (AOB) revealed by PCR amplification of amoA gene in a polyacrylamide transportation system of an oilfield. Int Biodeterior Biodegradation 115:110–118

    Article  CAS  Google Scholar 

  • Limei S, Yuanfeng C, Kong Yu, Yang F (2016) Changes in structure and element composition of mucilage sheath of Microcystis colony during the bioom decline period. J Lake Sci 28:944–950

    Article  Google Scholar 

  • Liu FH, Lin GH, Gao G, Qin BQ, Zhang JS, Zhao GP, Zhou ZH, Shen JH (2010) Bacterial and archaeal assemblages in sediments of a large shallow freshwater lake, Lake Taihu, as revealed by denaturing gradient gel electrophoresis. J Appl Microbiol 106:1022–1032

    Article  CAS  Google Scholar 

  • Lund JWG, Kipling C, Cren EDL (1958) The inverted microscope method of estimating algal numbers and the statistical basis of estimations by counting. Hydrobiologia 11(2):143–170

    Article  Google Scholar 

  • Ma J, Qin B, Paerl HW, Brookes JD, Hall NS, Shi K, Zhou Y, Guo J, Zhe L, Hai X (2016) The persistence of cyanobacterial (Microcystis spp.) blooms throughout winter in Lake Taihu, China. Limnol Oceanogr 61:711–722

    Article  Google Scholar 

  • Ma Y, Wei T, Jiao L, Liu C, Jin L, Liu J (2018) Response of ammonia-oxidizing betaproteobacteria to short-term fertilization in a salt marsh in china. Chin J Oceanol Limnol 2:1–11

    CAS  Google Scholar 

  • Naponelli V, Noiriel A, Ziemak MJ, Beverley SM, Lye LF, Plume AM et al (2008) Phylogenomic and functional analysis of pterin-4a-carbinolamine dehydratase family (cog2154) proteins in plants and microorganisms. Plant Physiol 146:1515–1527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Natale DA, Shankavaram UT, Galperin MY (2000) Towards understanding the first genome sequence of a crenarchaeon by genome annotation using clusters of orthologous groups of proteins (COGs). Genome Biol 1(5):1–19

    Article  Google Scholar 

  • Neil JM, Davis TW, Burford MA, Gobler CJ (2012) The rise of harmful cyanobacteria blooms: the potential roles of eutrophication and climate change. Harmful Algae 14:313–334

    Article  CAS  Google Scholar 

  • Niu Y, Shen H, Chen J, Xie P, Yang X, Tao M et al (2011) Phytoplankton community succession shaping bacterioplankton community composition in Lake Taihu, China. Water Res 45(14):4169–4182

    Article  CAS  PubMed  Google Scholar 

  • Oliver RL, Ganf GG (2000) Freshwater blooms. In: Whitton BA, Potts M (eds) The ecology of cyanobacteria. Springer, Dordrecht, pp 149–194

    Google Scholar 

  • Park HD, Sasaki Y, Maruyama T, Yanagisawa E, Hiraishi A, Kato K (2010) Degradation of the cyanobacterial hepatotoxin microcystin by a new bacterium isolated from a hypertrophic lake. Environ Toxicol 16:337–343

    Article  CAS  Google Scholar 

  • Popoff MR (2018) Botulinum neurotoxins: Still a privilege of clostridia? Cell Host Microbe 23(2):145–146

    Article  CAS  PubMed  Google Scholar 

  • Purkhold U, Pommerening-Röser A, Juretschko S, Schmid MC, Koops HP, Wagner M (2000) Phylogeny of all recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis: implications for molecular diversity surveys. Appl Environ Microbiol 66:5368–5382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qin B, Xu P, Wu Q, Luo L, Zhang Y (2007) Environmental issues of Lake Taihu, China. Hydrobiologia 581:3–14

    Article  CAS  Google Scholar 

  • Qin B, Zhu G, Gao G, Zhang Y, Wei L, Paerl HW, Carmichael WW (2010) A drinking water crisis in Lake Taihu, China: linkage to climatic variability and lake management. Environ Manag 45:105–112

    Article  Google Scholar 

  • Qing ZX, Yan YL, Qiang YD, Cheng WR, Cai LX, Qiang QB (2008) Vertical distribution of physicochemical characteristics and the microbial diversity in different spatial sediments samples in Lake Taihu. Environ Sci 29(29):3537–3545

    Google Scholar 

  • Reynolds CS, Jaworski GHM, Cmiech HA, Leedale GF (1981) On the annual cycle of the blue-green alga Microcystis Aeruginosa Kutz. Emend. Elenkin. Philos Trans R Soc B Biological Sci 293(1068):419–477

    Google Scholar 

  • Schmid M, Twachtmann U, Klein M, Strous M, Juretschko S, Jetten M, Metzger JW, Schleifer KH, Wagner M (2000) Molecular evidence for genus level diversity of bacteria capable of catalyzing anaerobic ammonium oxidation. Syst Appl Microbiol 23:93–106

    Article  CAS  PubMed  Google Scholar 

  • Shao K, Gao G, Wang Y, Tang X, Qin B (2013) Vertical diversity of sediment bacterial communities in two different trophic states of the eutrophic Lake Taihu, China. J Environ Sci China 25:1186–1194

    Article  CAS  PubMed  Google Scholar 

  • Shen H, Niu Y, Xie P, Tao M, Yang X (2011) Morphological and physiological changes in Microcystis aeruginosa as a result of interactions with heterotrophic bacteria. Freshw Biol 56(6):1065–1080

    Article  CAS  Google Scholar 

  • Smith JL, Boyer GL, Zimba PV (2008) A review of cyanobacterial odorous and bioactive metabolites: impacts and management alternatives in aquaculture. Aquaculture 280:5–20

    Article  CAS  Google Scholar 

  • Tang FHM, Maggi F (2017) Living microorganisms change the information (Shannon) content of a geophysical system. Sci Rep 7(1):3320

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tripathy S, Maiti NK (2014) Construction of Geobacillus thermoglucosidasius cDNA library and analysis of genes expressed in response to heat stress. Mol Biol Rep 41:1639–1644

    Article  CAS  PubMed  Google Scholar 

  • Verhamme DT, Prosser JI, Nicol GW (2011) Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J 5:1067

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wan Y, Bai Y, He J, Zhang Y, Ruan X (2017) Temporal and spatial variations of aquatic environmental characteristics and sediment bacterial community in five regions of Lake Taihu. Aquat Ecol 51(3):1–16

    Article  CAS  Google Scholar 

  • Wang Y, Chen F (2008) Decomposition and phosphorus release from four different size fractions of Microcystis spp. taken from Lake Taihu. China J Environ Sci 20:891–896

    Article  Google Scholar 

  • Whitman RL, Nevers MB, Byappanahalli MN (2006) Examination of the watershed-wide distribution of Escherichia coli along southern Lake Michigan: an integrated approach. Appl Environ Microbiol 72(11):7301–7310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson AE, Kaul RB, Sarnelle O (2010) Growth rate consequences of coloniality in a harmful phytoplankter. PLoS ONE 5(1):1–8

    Google Scholar 

  • Wobus A, Bleul C, Maassen S et al (2003) Microbial diversity and functional characterization of sediments from reservoirs of different trophic state. FEMS Microbiol Ecol 46(3):331–347

    Article  CAS  PubMed  Google Scholar 

  • Xia L, Lu X, Chen Y (2011) The effects of temperature and nutrient ratios on Microcystis blooms in Lake Taihu, China: an 11-year investigation. Harmful Algae 10:337–343

    Article  CAS  Google Scholar 

  • Xiao M, Li M, Reynolds CS (2018) Colony formation in the cyanobacterium microcystis. Biol Rev 93(3):1399–1420

    Article  PubMed  Google Scholar 

  • Xie LQ, Xie P, Tang HJ (2003) Enhancement of dissolved phosphorus release from sediment to lake water by Microcystis blooms—an enclosure experiment in a hyper-eutrophic, subtropical Chinese lake. Environ Pollut 122:391–399

    Article  CAS  PubMed  Google Scholar 

  • Xing P, Guo L, Tian W, Wu QL (2010) Novel clostridium populations involved in the anaerobic degradation of microcystis blooms. ISME J 5(5):792–800

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yin-Gang X, Fei L, Meng S, Xiao-Dong J, Jin-Ju G, Jia-Quan T et al (2018) Community structure and influencing factors of bacterioplankton in spring in Zhushan bay, Lake Taihu. Environ Sci 39(3):1151

    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 

  • Zeng J, Zhao DY, Huang R, Wu QL (2012) Abundance and community composition of ammonia-oxidizing archaea and bacteria in two different zones of Lake Taihu. Can J Microbiol 58(8):1018–1026

    Article  CAS  PubMed  Google Scholar 

  • Zengler K, Zaramela LS (2018) The social network of microorganisms—how auxotrophies shape complex communities. Nat Rev Microbiol 16:383–390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang XJ, Chen C, Ding JQ, Hou A, Li Y, Niu ZB, Su XY, Xu YJ, Laws EA (2010) The 2007 water crisis in Wuxi, China: analysis of the origin. J Hazard Mater 182:130–135

    Article  CAS  PubMed  Google Scholar 

  • Zhao D, Xu H, Zeng J, Cao X, Huang R, Shen F et al (2017) Community composition and assembly processes of the free-living and particle-attached bacteria in Taihu Lake. FEMS Microbiol Ecol 93(6):fix062

    Article  CAS  Google Scholar 

  • Zohary T, Fishbein T, Shlichter M, Naselli-Flores L (2017) Larger cell or colony size in winter, smaller in summer—a pattern shared by many species of Lake Kinneret phytoplankton. Inland Waters 7(2):200–209

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was financially supported by ABA Chemicals for funding support and National Science and Technology Major Project (2017ZX07204005-04). We thank the anonymous reviewers for their valuable comments and suggestions. Further thanks to Ms. Zhang Pengying for modifying the images presented in this article.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Jian He or Zheng Zheng.

Additional information

Handling Editor: Télesphore Sime-Ngando.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 1055 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, W., Gu, P., Zhu, W. et al. Phenotype changes of cyanobacterial and microbial distribution characteristics of surface sediments in different periods of cyanobacterial blooms in Taihu Lake. Aquat Ecol 54, 591–607 (2020). https://doi.org/10.1007/s10452-020-09761-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10452-020-09761-1

Keywords

Navigation