Abstract
Bacterial communities play an important role in the biogeochemical cycle in reservoir ecosystems. However, the dynamic changes in both planktonic and sediment bacterial communities in a highly regulated dam reservoir remain unclear. This study investigated the temporal distribution patterns of bacterial communities in a transition section of the Three Gorges Reservoir (TGR) using Illumina MiSeq sequencing. Results suggested that in comparison to the planktonic bacteria, sediment bacteria contributed more to the reservoir microbial communities, accounting for 97% of the 7434 OTUs. The Shannon diversity index in the water (3.22~5.68) was generally lower than that in the sediment (6.72~7.56). In the high water level period (January and March), Proteobacteria, Actinobacteria, Cyanobacteria, and Firmicutes were the most abundant phyla, whereas in the low water level period (May, July, and September), the dominant phyla were Proteobacteria, Actinobacteria, and Bacteroidetes. Sediment samples were dominated by Proteobacteria, Chloroflexi, and Acidobacteria. Principal coordinate analysis of the bacterioplankton communities showed greater sensitivity to monthly changes than that of the sediment bacterial communities. Network analysis suggested that in comparison to planktonic bacterial communities, sediment bacterial communities were more complex and stable. The linear relationship between the CH4/CO2 ratio, water level, and relative abundance of methanotrophs highlighted the potential methane-oxidizing process in the mid-part of the TGR. Moreover, the potential impact of dam regulation on the bacterial communities was revealed by the significant relationship between abundant phyla and the inflow of the TGR.
Key points
• Bacterioplankton communities showed great sensitivity to monthly changes.
• Potential methane-oxidizing process was revealed in this representative area.
• Water inflow regulated by dam has significant effects on dominant bacterioplankton.
Similar content being viewed by others
References
Borrel G, Jezequel D, Biderre-Petit C, Morel-Desrosiers N, Morel JP, Peyret P, Fonty G, Lehours AC (2011) Production and consumption of methane in freshwater lake ecosystems. Res Microbiol 162(9):832–847. https://doi.org/10.1016/j.resmic.2011.06.004
Bosse U, Frenzel P, Conrad R (1993) Inhibition of methane oxidation by ammonium in the surface-layer of a littoral sediment. FEMS Microbiol Ecol 13(2):123–134. https://doi.org/10.1016/0168-6496(93)90030-b
Bowman J (2006) The methanotrophs — the families Methylococcaceae and Methylocystaceae. 5:266–289 https://doi.org/10.1007/0-387-30745-1_15
Bussmann I, Hackbusch S, Schaal P, Wichels A (2017) Methane distribution and oxidation around the Lena Delta in summer 2013. Biogeosciences 14(21):4985–5002. https://doi.org/10.5194/bg-14-4985-2017
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Tumbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336. https://doi.org/10.1038/nmeth.f.303
Chen Y, Liu Y, Wang X (2017) Spatiotemporal variation of bacterial and archaeal communities in sediments of a drinking reservoir, Beijing, China. Appl Microbiol Biotechnol 101(8):3379–3391. https://doi.org/10.1007/s00253-016-8019-1
Chen ZB, Zhou ZY, Peng X, Xiang H, Xiang SN, Jiang ZX (2013) Effects of wet and dry seasons on the aquatic bacterial community structure of the Three Gorges Reservoir. World J Microbiol Biotechnol 29(5):841–853. https://doi.org/10.1007/s11274-012-1239-3
Clark DR, Ferguson RMW, Harris DN, Matthews Nicholass KJ, Prentice HJ, Randall KC, Randell L, Warren SL, Dumbrell AJ (2018) Streams of data from drops of water: 21st century molecular microbial ecology. Wires Water 5(4):e1280. https://doi.org/10.1002/wat2.1280
Cole JK, Peacock JP, Dodsworth JA, Williams AJ, Thompson DB, Dong HL, Wu G, Hedlund BP (2013) Sediment microbial communities in Great Boiling Spring are controlled by temperature and distinct from water communities. ISME J 7(4):718–729. https://doi.org/10.1038/ismej.2012.157
Coyte KZ, Schluter J, Foster KR (2015) The ecology of the microbiome: networks, competition, and stability. Science 350(6261):663–666. https://doi.org/10.1126/science.aad2602
Crevecoeur S, Ruiz-Gonzalez C, Prairie YT, del Giorgio PA (2019) Large-scale biogeography and environmental regulation of methanotrophic bacteria across boreal inland waters. Mol Ecol 28(18):4181–4196. https://doi.org/10.1111/mec.15223
Crevecoeur S, Vincent WF, Comte J, Matveev A, Lovejoy C (2017) Diversity and potential activity of methanotrophs in high methane-emitting permafrost thaw ponds. PLoS One 12(11):e0188223. https://doi.org/10.1371/journal.pone.0188223
Crump BC, Hobbie JE (2005) Synchrony and seasonality in bacterioplankton communities of two temperate rivers. Limnol Oceanogr 50(6):1718–1729. https://doi.org/10.4319/lo.2005.50.6.1718
Crump BCPB, Raymond PA, RMW A, Rinehart A, JW MC, et al. (2009) Circumpolar synchrony in big river bacterioplankton. PNAS 106:21208–21212. https://doi.org/10.1073/pnas.0906149106
Dean JF, Middelburg JJ, Rockmann T, Aerts R, Blauw LG, Egger M, Jetten MSM, de Jong AEE, Meisel OH, Rasigraf O, Slomp CP, in’t Zandt MH, Dolman AJ (2018) Methane feedbacks to the global climate system in a warmer world. Rev Geophys 56(1):207–250. https://doi.org/10.1002/2017rg000559
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10(10):996–998. https://doi.org/10.1038/nmeth.2604
Feng BW, Li XR, Wang JH, Hu ZY, Meng H, Xiang LY, Quan ZX (2009) Bacterial diversity of water and sediment in the Changjiang estuary and coastal area of the East China Sea. FEMS Microbiol Ecol 70(2):80–92. https://doi.org/10.1111/j.1574-6941.2009.00772.x
Ferry JG, Lessner DJ (2010) Methanogenesis in marine sediments. Ann N Y Acad Sci 1125(1):147–157. https://doi.org/10.1196/annals.1419.007
Frenzel P, Thebrath B, Conrad R (1990) Oxidation of methane in the oxic surface layer of a deep lake sediment (Lake Constance). FEMS Microbiol Lett 73:149–158. https://doi.org/10.1016/0378-1097(90)90661-9
Fuhrman JA, Steele JA, Hewson I, Schwalbach MS, Brown MV, Green JL, Brown JH (2008) A latitudinal diversity gradient in planktonic marine bacteria. PNAS 105(22):7774–7778. https://doi.org/10.1073/pnas.0803070105
Gkelis S, Papadimitriou T, Zaoutsos N, Leonardos I (2014) Anthropogenic and climate-induced change favors toxic cyanobacteria blooms: evidence from monitoring a highly eutrophic, urban mediterranean lake. Harmful Algae 39:322–333. https://doi.org/10.1016/j.hal.2014.09.002
He R, Wooller MJ, Pohlman JW, Quensen J, Tiedje JM, Leigh MB (2012) Shifts in identity and activity of methanotrophs in arctic lake sediments in response to temperature changes. Appl Environ Microbiol 78(13):4715–4723. https://doi.org/10.1128/AEM.00853-12
Henson MW, Hanssen J, Spooner G, Fleming P, Pukonen M, Stahr F, Thrash JC (2018) Nutrient dynamics and stream order influence microbial community patterns along a 2914 kilometer transect of the Mississippi River. Limnol Oceanogr 63(5):1837–1855. https://doi.org/10.1002/lno.10811
Horz HP, Rich V, Avrahami S, Bohannan BJM (2005) Methane-oxidizing bacteria in a California upland grassland soil: diversity and response to simulated global change. Appl Environ Microbiol 71(5):2642–2652. https://doi.org/10.1128/aem.71.5.2642-2652.2005
Ju LH, Yang J, Liu LM, Wilkinson DM (2014) Diversity and distribution of freshwater testate amoebae (protozoa) along latitudinal and trophic gradients in China. Microb Ecol 68(4):657–670. https://doi.org/10.1007/s00248-014-0442-1
Kasalicky V, Jezbera J, Hahn MW, Simek K (2013) The diversity of the Limnohabitans genus, an important group of freshwater bacterioplankton, by characterization of 35 isolated strains. PLoS One 8(3):13. https://doi.org/10.1371/journal.pone.0058209
Klaver G, van Os B, Negrel P, Petelet-Giraud E (2007) Influence of hydropower dams on the composition of the suspended and riverbank sediments in the Danube. Environ Pollut 148(3):718–728. https://doi.org/10.1016/j.envpol.2007.01.037
Knoblauch C, Zimmermann U, Blumenberg M, Michaelis W, Pfeiffer EM (2008) Methane turnover and temperature response of methane-oxidizing bacteria in permafrost-affected soils of northeast Siberia. Soil Biol Biochem 40(12):3004–3013. https://doi.org/10.1016/j.soilbio.2008.08.020
Kraemer BM, Chandra S, Dell AI, Dix M, Kuusisto E, Livingstone DM, Schladow SG, Silow E, Sitoki LM, Tamatamah R, McIntyre PB (2017) Global patterns in lake ecosystem responses to warming based on the temperature dependence of metabolism. Glob Change Biol 23(5):1881–1890. https://doi.org/10.1111/gcb.13459
Landi P, Minoarivelo HO, Brännström Å, Hui C, Dieckmann U (2018) Complexity and stability of ecological networks: a review of the theory. Popul Ecol 60(4):319–345. https://doi.org/10.1007/s10144-018-0628-3
Lehner B, Liermann CR, Revenga C, Vörösmarty C, Fekete B, Crouzet P, Döll P, Endejan M, Frenken K, Magome J, Nilsson C, Robertson JC, Rödel R, Sindorf N, Wisser D (2011) High-resolution mapping of the world’s reservoirs and dams for sustainable river-flow management. Front Ecol Environ 9(9):494–502. https://doi.org/10.1890/100125
Li X, Guo S, Liu P, Chen G (2010) Dynamic control of flood limited water level for reservoir operation by considering inflow uncertainty. J Hydrol 391(1–2):124–132. https://doi.org/10.1016/j.jhydrol.2010.07.011
Li Y, Gao Y, Zhang W, Wang C, Wang P, Niu L, Wu H (2019) Homogeneous selection dominates the microbial community assembly in the sediment of the Three Gorges Reservoir. Sci Total Environ 690:50–60. https://doi.org/10.1016/j.scitotenv.2019.07.014
Li Z, Lu L, Guo J, Yang J, Zhang J, He B, Xu L (2017) Responses of spatial-temporal dynamics of bacterioplankton community to large-scale reservoir operation: a case study in the Three Gorges Reservoir, China. Sci Rep 7:42469. https://doi.org/10.1038/srep42469
Li Z, Lu L, Lv P, Zhang Z, Guo J (2020) Imbalanced stoichiometric reservoir sedimentation regulates methane accumulation in China’s Three Gorges Reservoir. Water Resour Res 56:26447. https://doi.org/10.1029/2019WR026447
Li Z, Zhang ZY, Lin CX, Chen YB, Wen AB, Fang F (2016) Soil-air greenhouse gas fluxes influenced by farming practices in reservoir drawdown area: a case at the Three Gorges Reservoir in China. J Environ Manag 181:64–73. https://doi.org/10.1016/j.jenvman.2016.05.080
Liu KL, Wong TT (2013) Naive bayesian classifiers with multinomial models for rRNA taxonomic assignment. IEEE-ACM Trans Comput Biol Bioinform 10(5):1334–1339. https://doi.org/10.1109/tcbb.2013.114
Liu L, Chen H, Liu M, Yang JR, Xiao P, Wilkinson DM, Yang J (2019a) Response of the eukaryotic plankton community to the cyanobacterial biomass cycle over 6 years in two subtropical reservoirs. ISME J 13(9):2196–2208. https://doi.org/10.1038/s41396-019-0417-9
Liu L, Liu DF, Johnson DM, Yi ZQ, Huang YL (2012) Effects of vertical mixing on phytoplankton blooms in Xiangxi Bay of Three Gorges Reservoir: implications for management. Water Res 46(7):2121–2130. https://doi.org/10.1016/j.watres.2012.01.029
Liu LM, Yang J, Yu Z, Wilkinson DM (2015) The biogeography of abundant and rare bacterioplankton in the lakes and reservoirs of China. ISME J 9(9):2068–2077. https://doi.org/10.1038/ismej.2015.29
Liu M, Liu L, Chen H, Yu Z, Yang JR, Xue Y, Huang B, Yang J (2019b) Community dynamics of free-living and particle-attached bacteria following a reservoir Microcystis bloom. Sci Total Environ 660:501–511. https://doi.org/10.1016/j.scitotenv.2018.12.414
Liu M, Xue Y, Yang J (2019c) Rare plankton subcommunities are far more affected by DNA extraction kits than abundant plankton. Front Microbiol 10:454. https://doi.org/10.3389/fmicb.2019.00454
Liu T, Zhang AN, Wang J, Liu S, Jiang X, Dang C, Ma T, Liu S, Chen Q, Xie S, Zhang T, Ni J (2018) Integrated biogeography of planktonic and sedimentary bacterial communities in the Yangtze River. Microbiome 6(1):16. https://doi.org/10.1186/s40168-017-0388-x
Lu L, Zou X, Yang J, Xiao Y, Wang Y, Guo J, Li Z (2020) Biogeography of eukaryotic plankton communities along the upper Yangtze River: the potential impact of cascade dams and reservoirs. J Hydrol 590:125495. https://doi.org/10.1016/j.jhydrol.2020.125495
Maavara T, Chen Q, Van Meter K, Brown LE, Zhang J, Ni J, Zarfl C (2020) River dam impacts on biogeochemical cycling. Nat Rev Earth Environ 1(2):103–116. https://doi.org/10.1038/s43017-019-0019-0
Madsen EL (2011) Microorganisms and their roles in fundamental biogeochemical cycles. Curr Opin Biotechnol 22(3):456–464. https://doi.org/10.1016/j.copbio.2011.01.008
Marshall BEJFJR (1981) The decline of salvinia-molesta on Lake Kariba Zimbabwe. Hydrobiologia 83:477–484. https://doi.org/10.1007/bf02187043
Martins G, Terada A, Ribeiro DC, Corral AM, Brito AG, Smets BF, Nogueira R (2011) Structure and activity of lacustrine sediment bacteria involved in nutrient and iron cycles. FEMS Microbiol Ecol 77(3):666–679. https://doi.org/10.1111/j.1574-6941.2011.01145.x
Matoušů A, Osudar R, Šimek K, Bussmann I (2016) Methane distribution and methane oxidation in the water column of the Elbe estuary, Germany. Aquat Sci 79(3):443–458. https://doi.org/10.1007/s00027-016-0509-9
Murrell JC, Jetten MS (2009) The microbial methane cycle. Environ Microbiol Rep 1(5):279–284. https://doi.org/10.1111/j.1758-2229.2009.00089.x
Nyirabuhoro P, Liu M, Xiao P, Liu L, Yu Z, Wang L, Yang J (2020) Seasonal variability of conditionally rare taxa in the water column bacterioplankton community of subtropical reservoirs in China. Microb Ecol 80(1):14–26. https://doi.org/10.1007/s00248-019-01458-9
Pomeroy LR, Wiebe WJ (2001) Temperature and substrates as interactive limiting factors for marine heterotrophic bacteria. Aquat Microb Ecol 23(2):187–204. https://doi.org/10.3354/ame023187
Protection ME (2012) Soil-determination of ammonium,nitrite and nitrate by extraction with potassium chloride solution-spectrophotometric methods. Beijing: China Environmental Science Press (HJ 634–2012)
Qin Y, Zhang Y, Li Z, Ma J (2018) CH4 fluxes during the algal bloom in the Pengxi River. Environment Science (Chinese Edition) 39(04):1578–1588. https://doi.org/10.13227/j.hjkx.201706044
Ren Q, Li C, Yang W, Song H, Ma P, Wang C, Schneider RL, Morreale SJ (2018) Revegetation of the riparian zone of the Three Gorges Dam Reservoir leads to increased soil bacterial diversity. Environ Sci Pollut Res 25(24):23748–23763. https://doi.org/10.1007/s11356-018-2333-3
Roland FAE, Darchambeau F, Morana C, Bouillon S, Borges AV (2017) Emission and oxidation of methane in a meromictic, eutrophic and temperate lake (Dendre, Belgium). Chemosphere 168:756–764. https://doi.org/10.1016/j.chemosphere.2016.10.138
Rottjers L, Faust K (2018) From hairballs to hypotheses-biological insights from microbial networks. FEMS Microbiol Rev 42(6):761–780. https://doi.org/10.1093/femsre/fuy030
Ruiz-González C, Proia L, Ferrera I, Gasol JM, Sabater S (2013) Effects of large river dam regulation on bacterioplankton community structure. FEMS Microbiol Ecol 84(2):316–331. https://doi.org/10.1111/1574-6941.12063
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12(6):18. https://doi.org/10.1186/gb-2011-12-6-r60
Society ACCoCS (1982) Methods for routine analysis of soil agricultural chemistry. Science Press, Beijing
Stegen JC, Lin X, Konopka AE, Fredrickson JK (2012) Stochastic and deterministic assembly processes in subsurface microbial communities. ISME J 6(9):1653–1664. https://doi.org/10.1038/ismej.2012.22
Straškraba M (1999) Retention time as a key variable of reservoir limnology. In: Theoretical reservoir ecology and its applications (eds Tundisi JG & Straškraba M). International Institute of Ecology, Brazilian Academy of Sciences and Backhuys Publishers, pp 385–410
Sun Z, Li G, Wang C, Jing Y, Zhu Y, Zhang S, Liu Y (2014) Community dynamics of prokaryotic and eukaryotic microbes in an estuary reservoir. Sci Rep 4:6966. https://doi.org/10.1038/srep06966
Thornton KW, Kimmel BL, Payne FE (1990) Reservoir limnology: ecological perspectives (John Wiley & Sons)
Walters W, Hyde ER, Berg-Lyons D, Ackermann G, Humphrey G, Parada A, Gilbert JA, Jansson JK, Caporaso JG, Fuhrman JA, Apprill A, Knight R (2016) Improved bacterial 16S rRNA gene (V4 and V4-5) and fungal internal transcribed spacer marker gene primers for microbial community surveys. mSystems 1(1):9–15. https://doi.org/10.1128/mSystems.00009-15
Wang C, Xiao S, Li Y, Zhong H, Li X, Peng F (2014) Methane formation and consumption processes in Xiangxi Bay of the Three Gorges Reservoir. Sci Rep 4:4449. https://doi.org/10.1038/srep04449
Wang Y, Lu L, Hong Y, Wu J, Zhu G, Ye F, Li Z (2020) Divergent responses of taxonomic and predicted functional profiles of bacterioplankton to reservoir impoundment. Environ Res 182:109083. https://doi.org/10.1016/j.envres.2019.109083
Wang YM, Liu LM, Chen HH, Yang J (2015) Spatiotemporal dynamics and determinants of planktonic bacterial and microeukaryotic communities in a Chinese subtropical river. Appl Microbiol Biotechnol 99(21):9255–9266. https://doi.org/10.1007/s00253-015-6773-0
Winton RS, Calamita E, Wehrli B (2019) Reviews and syntheses: dams, water quality and tropical reservoir stratification. Biogeosciences 16(8):1657–1671. https://doi.org/10.5194/bg-16-1657-2019
Xiang Y, Wang Y, Zhang C, Shen H, Wang D (2018) Water level fluctuations influence microbial communities and mercury methylation in soils in the Three Gorges Reservoir, China. J Environ Sci 68:206–217. https://doi.org/10.1016/j.jes.2018.03.009
Xu Y, Cai Q, Shao M, Han X (2011) Patterns of asynchrony for phytoplankton fluctuations from reservoir mainstream to a tributary bay in a giant dendritic reservoir (Three Gorges Reservoir, China). Aquat Sci 74(2):287–300. https://doi.org/10.1007/s00027-011-0221-8
Yan Q, Bi Y, Deng Y, He ZL, Wu LY, Van Nostrand JD, Shi Z, Li JJ, Wang X, Hu ZY, Yu YH, Zhou JH (2015) Impacts of the Three Gorges Dam on microbial structure and potential function. Sci Rep 5:8605. https://doi.org/10.1038/srep08605
Zeglin LH (2015) Stream microbial diversity in response to environmental changes: review and synthesis of existing research. Front Microbiol 6:454. https://doi.org/10.3389/fmicb.2015.00454
Zhang W, Gu J, Li Y, Lin L, Wang P, Wang C, Qian B, Wang H, Niu L, Wang L, Zhang H, Gao Y, Zhu M, Fang S (2019) New insights into sediment transport in interconnected river-lake systems through tracing microorganisms. Environ Sci Technol 53(8):4099–4108. https://doi.org/10.1021/acs.est.8b07334
Acknowledgments
The authors thank Ziwei Wang, Yuyang Zhang, and Zhengmian Liu who participated in field sampling.
Funding
This study was funded by the National Natural Science Foundation of China (no. 51861125204 and 91647208) and National Key Research and Development Plan of China (grant number 2017YFC0404705). The Chongqing Bureau of Science and Technology also provided partial financial support of the study through the following research projects: project no. cstc2020jscx-msxmX0121, and no. cstc2020jcyj-jqX0010.
Author information
Authors and Affiliations
Contributions
YQ and QT investigated, studied, and wrote the original manuscript. LL provided the frame, the research goal of article, and supervised this work. YW revised the manuscript and supervised this work. II revised the manuscript. ZL was responsible for proofreading and reviewed article. All authors read and approved the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(DOCX 684 kb)
Rights and permissions
About this article
Cite this article
Qin, Y., Tang, Q., Lu, L. et al. Changes in planktonic and sediment bacterial communities under the highly regulated dam in the mid-part of the Three Gorges Reservoir. Appl Microbiol Biotechnol 105, 839–852 (2021). https://doi.org/10.1007/s00253-020-11047-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-020-11047-3