Cite this paper:
Pinhua XIA, Guoqing LI, Xianfei HUANG, Lei SHI, Xin DU, Tao LIN. Temporal characteristics of algae-denitrifying bacteria co-occurrence patterns and denitrifier assembly in epiphytic biofilms on submerged macrophytes in Caohai Lake, SW China[J]. Journal of Oceanology and Limnology, 2023, 41(6): 2276-2291

Temporal characteristics of algae-denitrifying bacteria co-occurrence patterns and denitrifier assembly in epiphytic biofilms on submerged macrophytes in Caohai Lake, SW China

Pinhua XIA, Guoqing LI, Xianfei HUANG, Lei SHI, Xin DU, Tao LIN
Guizhou Province Key Laboratory for Information System of Mountainous Areas and Protection of Ecological Environment, Guizhou Normal University, Guiyang 550001, China
Denitrifying bacteria in epiphytic biofilms play a crucial role in nitrogen cycle in aquatic habitats. However, little is known about the connection between algae and denitrifying bacteria and their assembly processes in epiphytic biofilms. Epiphytic biofilms were collected from submerged macrophytes (Patamogeton lucens and Najas marina L.) in the Caohai Lake, Guizhou, SW China, from July to November 2020 to: (1) investigate the impact of abiotic and biotic variables on denitrifying bacterial communities; (2) investigate the temporal variation of the algae-denitrifying bacteria co-occurrence networks; and (3) determine the contribution of deterministic and stochastic processes to the formation of denitrifying bacterial communities. Abiotic and biotic factors influenced the variation in the denitrifying bacterial community, as shown in the Mantel test. The co-occurrence network analysis unveiled intricate interactions among algae to denitrifying bacteria. Denitrifying bacterial community co-occurrence network complexity (larger average degrees representing stronger network complexity) increased continuously from July to September and decreased in October before increasing in November. The co-occurrence network complexity of the algae and nirS-encoding denitrifying bacteria tended to increase from July to November. The co-occurrence network complexity of the algal and denitrifying bacterial communities was modified by ammonia nitrogen (NH4+-N) and total phosphorus (TP), pH, and water temperature (WT), according to the ordinary least-squares (OLS) model. The modified stochasticity ratio (MST) results reveal that deterministic selection dominated the assembly of denitrifying bacterial communities. The influence of environmental variables to denitrifying bacterial communities, as well as characteristics of algal-bacterial co-occurrence networks and the assembly process of denitrifying bacterial communities, were discovered in epiphytic biofilms in this study. The findings could aid in the appropriate understanding and use of epiphytic biofilms denitrification function, as well as the enhancement of water quality.
Key words:    denitrifying bacteria    epiphytic biofilms    co-occurrence networks    submerged macrophytes    community assembly   
Received: 2022-04-13   Revised:
PDF (7490 KB) Free
Print this page
Add to favorites
Email this article to others
Articles by Pinhua XIA
Articles by Guoqing LI
Articles by Xianfei HUANG
Articles by Lei SHI
Articles by Xin DU
Articles by Tao LIN
Chen J, Ying G G, Liu Y S et al.2017.Nitrogen removal and its relationship with the nitrogen-cycle genes and microorganisms in the horizontal subsurface flow constructed wetlands with different design parameters.Journal of Environmental Science and Health, Part A-Toxic/Hazardous Substances & Environmental Engineering, 52(8):804-818,
Chen Q L, Hu H W, Yan Z Z et al.2021.Deterministic selection dominates microbial community assembly in termite mounds.Soil Biology & Biochemistry, 152:108073,
Chen W D, Wen D H.2021.Archaeal and bacterial communities assembly and co-occurrence networks in subtropical mangrove sediments under Spartina alterniflora invasion.Environmental Microbiome, 16:10,
Chen X C, Huang Y Y, Chen G Q et al.2018.The secretion of organics by living Microcystis under the dark/anoxic condition and its enhancing effect on nitrate removal.Chemosphere, 196:280-287,
Cheng S, Huai J, Zhong F et al.2021.Enhancing denitrification in constructed wetland with algae addition.Environmental Science and Pollution Research, 29:1949-1960,
Dai H T, Zhu R B, Sun B W et al.2020.Effects of sea animal activities on tundra soil denitrification and nirS- and nirK-encoding denitrifier community in maritime Antarctica.Frontiers in Microbiology, 11:573302,
D'Amen M, Mod H K, Gotelli N J et al.2018.Disentangling biotic interactions, environmental filters, and dispersal limitation as drivers of species co-occurrence.Ecography, 41(8):1233-1244,
Deng J, Chen X C, Huang Y Y et al.2020.Biogeochemical cycling processes associated with cyanobacterial aggregates.Acta Microbiologica Sinica, 60(9):1922-1940, Chinese with English abstract)
Desbois A P, Lebl T, Yan L M et al.2008.Isolation and structural characterisation of two antibacterial free fatty acids from the marine diatom, Phaeodactylum tricornutum.Applied Microbiology and Biotechnology, 81(4):755-764,
Espeland E M, Francoeur S N, Wetzel R G.2001.Influence of algal photosynthesis on biofilm bacterial production and associated glucosidase and xylosidase activities.Microbial Ecology, 42(4):524-530,
Feng J, Wang F, Xie S L.2011.Structure and dynamics of the periphytic algae of Jinyang Lake in Shanxi Province, North China.Acta Ecologica Sinica, 31(6):310-316,
Fozia N, Zheng Y L, Hou L J et al.2020.Community dynamics and activity of nirS-harboring denitrifiers in sediments of the Indus River Estuary.Marine Pollution Bulletin, 153:110971,
Gonçalves A L, Pires J C M, Simões M.2017.A review on the use of microalgal consortia for wastewater treatment.Algal Research, 24:403-415,
Gubelit Y I, Grossart H P.2020.New methods, new concepts:what can be applied to freshwater periphyton? Frontiers in Microbiology, 11:1275,
Han B, Zhang S H, Zhang L S et al.2018.Characterization of microbes and denitrifiers attached to two species of floating plants in the wetlands of Lake Taihu.PLoS One, 13(11):e0207443,
He D, Ren L J, Wu Q L.2014.Contrasting diversity of epibiotic bacteria and surrounding bacterioplankton of a common submerged macrophyte, Potamogeton crispus, in freshwater lakes.FEMS Microbiology Ecology, 90(3):551-562,
He D, Ren L, Wu Q L.2020.Growing season drives the compositional changes and assembly processes of epiphytic bacterial communities of two submerged macrophytes in Taihu Lake.Fems Microbiology Ecology, 96(4):fiaa025,
He Q, Wang S, Hou W G et al.2021.Temperature and microbial interactions drive the deterministic assembly processes in sediments of hot springs.Science of the Total Environment, 772:145465,
Henderson R K, Baker A, Parsons S A et al.2008.Characterisation of algogenic organic matter extracted from cyanobacteria, green algae and diatoms.Water Research, 42(13):3435-3445,
Hong P, Wu X Q, Shu Y L et al.2019.Denitrification characterization of dissolved oxygen microprofiles in lake surface sediment through analyzing abundance, expression, community composition and enzymatic activities of denitrifier functional genes.AMB Express, 9(1):129,
Ishida C K, Arnon S, Peterson C G et al.2008.Influence of algal community structure on denitrification rates in periphyton cultivated on artificial substrata.Microbial Ecology, 56(1):140-152,
Jeong S Y, Yi T, Lee C H et al.2016.Spatiotemporal dynamics and correlation networks of bacterial and fungal communities in a membrane bioreactor.Water Research, 105:218-230,
Jones C M, Hallin S.2010.Ecological and evolutionary factors underlying global and local assembly of denitrifier communities.The ISME Journal, 4(5):633-641,
Kouzuma A, Watanabe K.2015.Exploring the potential of algae/bacteria interactions.Current Opinion in Biotechnology, 33:125-129,
Kraft B, Strous M, Tegetmeyer H E.2011.Microbial nitrate respiration-Genes, enzymes and environmental distribution.Journal of Biotechnology, 155(1):104-117,
Li C C, Wang L F, Ji S P et al.2021.The ecology of the plastisphere:microbial composition, function, assembly, and network in the freshwater and seawater ecosystems.Water Research, 202:117428,
Li G Q, Yan D B, Xia P H et al.2022.Community structure and assembly of denitrifying bacteria in epiphytic biofilms in a freshwater lake ecosystem.Journal of Oceanology and Limnology, 40(3):1039-1050,
Liu B B, Mørkved P T, Frostegård Å et al.2010.Denitrification gene pools, transcription and kinetics of NO, N2O and N2 production as affected by soil pH.FEMS Microbiology Ecology, 72(3):407-417,
Liu J Z, Wu Y H, Wu C X et al.2017.Advanced nutrient removal from surface water by a consortium of attached microalgae and bacteria:a review.Bioresource Technology, 241:1127-1137,
Liu S W, Yu H, Yu Y H et al.2022.Ecological stability of microbial communities in Lake Donghu regulated by keystone taxa.Ecological Indicators, 136:108695,
Liu Y S, Gong L X, Mu X Y et al.2020.Characterization and co-occurrence of microbial community in epiphytic biofilms and surface sediments of wetlands with submersed macrophytes.Science of the Total Environment, 715:136950,
Lu C C, Xie Z, Guo J B et al.2020.Chlorophyll as natural redox mediators for the denitrification process.International Biodeterioration & Biodegradation, 148:104895,
Lu H J, Chandran K, Stensel D.2014.Microbial ecology of denitrification in biological wastewater treatment.Water Research, 64:237-254,
Lyautey E, Hallin S, Teissier S et al.2013.Abundance, activity and structure of denitrifier communities in phototrophic river biofilms (River Garonne, France).Hydrobiologia, 716(1):177-187,
Miao L Z, Wang C Q, Adyel T M et al.2021.Periphytic biofilm formation on natural and artificial substrates:comparison of microbial compositions, interactions, and functions.Frontiers in Microbiology, 12:684903.
Moreno J, Vargas M A, Olivares H et al.1998.Exopolysaccharide production by the cyanobacterium Anabaena sp.ATCC 33047 in batch and continuous culture.Journal of Biotechnology, 60(3):175-182,
Mu X Y, Lv X Y, Liu W et al.2020.Biofilms attached to Myriophyllum spicatum play a dominant role in nitrogen removal in constructed wetland mesocosms with submersed macrophytes:evidence from 15N tracking, nitrogen budgets and metagenomics analyses.Environmental Pollution, 266:115203,
Natrah F M I, Bossier P, Sorgeloos P et al.2014.Significance of microalgal-bacterial interactions for aquaculture.Reviews in Aquaculture, 6(1):48-61,
Niederdorfer R, Fragner L, Yuan L et al.2021.Distinct growth stages controlled by the interplay of deterministic and stochastic processes in functional anammox biofilms.Water Research, 200:117225,
Pang S, Zhang S H, Lv X Y et al.2016.Characterization of bacterial community in biofilm and sediments of wetlands dominated by aquatic macrophytes.Ecological Engineering, 97:242-250,
Rajta A, Bhatia R, Setia H et al.2020.Role of heterotrophic aerobic denitrifying bacteria in nitrate removal from wastewater.Journal of Applied Microbiology, 128(5):1261-1278,
Ramanan R, Kang Z, Kim B H et al.2015.Phycosphere bacterial diversity in green algae reveals an apparent similarity across habitats.Algal Research, 8:140-144,
Saikia S K, Nandi S, Majumder S.2013.A review on the role of nutrients in development and organization of periphyton.Journal of Research in Biology, 3(1):780-788.
Shi R J, Xu S M, Qi Z H et al.2019.Seasonal patterns and environmental drivers of nirS- and nirK-encoding denitrifiers in sediments of Daya Bay, China.Oceanologia, 61(3):308-320,
Shrewsbury L H, Smith J L, Huggins D R et al.2016.Denitrifier abundance has a greater influence on denitrification rates at larger landscape scales but is a lesser driver than environmental variables.Soil Biology&Biochemistry, 103:221-231,
Song X, Lin T, Xia P H et al.2019.Algae composition and accumulation characteristics of heavy metals in epiphytic bioflioms of submerged macrophytes.Journal of Lake Sciences, 31(5):1268-1278,
Sun H, Pan B Z, He H R et al.2021.Assembly processes and co-occurrence relationships in the bacterioplankton communities of a large river system.Ecological Indicators, 126:107643,
Vila-Costa M, Bartrons M, Catalan J et al.2014.Nitrogen-cycling genes in epilithic biofilms of oligotrophic high-altitude lakes (Central Pyrenees, Spain).Microbial Ecology, 68(1):60-69,
Wang B H, Stirling E, He Z L et al.2021.Pollution alters methanogenic and methanotrophic communities and increases dissolved methane in small ponds.Science of the Total Environment, 801:149723,
Wang H L, Han J Q, Deng N et al.2019.Effects of the natural restoration time of abandoned farmland in a semiarid region on the soil denitrification rates and abundance and community structure of denitrifying bacteria.Applied Microbiology and Biotechnology, 103(4):1939-1951,
Wang Y M, Liu L M, Chen H H et al.2015.Spatiotemporal dynamics and determinants of planktonic bacterial and microeukaryotic communities in a Chinese subtropical river.Applied Microbiology and Biotechnology, 99(21):9255-9266,
Wang Y M, Pan J, Yang J et al.2020.Patterns and processes of free-living and particle-associated bacterioplankton and archaeaplankton communities in a subtropical river-bay system in South China.Limnology and Oceanography, 65(S1):S161-S179,
Wetzel R G.1983.Periphyton of Freshwater Ecosystems.Springer, Växjö, Sweden,
Wu H Y, Adams J M, Shi Y et al.2020.Depth-dependent patterns of bacterial communities and assembly processes in a typical red soil critical zone.Geomicrobiology Journal, 37(3):201-212,
Xia P H, Yan D B, Sun R G et al.2020.Community composition and correlations between bacteria and algae within epiphytic biofilms on submerged macrophytes in a plateau lake, southwest China.Science of the Total Environment, 727:138398,
Xiong C, Zhu Y G, Wang J T et al.2021.Host selection shapes crop microbiome assembly and network complexity.New Phytologist, 229(2):1091-1104,
Yan D B, Xia P H, Song X et al.2019.Community structure and functional diversity of epiphytic bacteria and planktonic bacteria on submerged macrophytes in Caohai Lake, southwest of China.Annals of Microbiology, 69(9):933-944,
Yan L Y, Zhang S H, Lin D et al.2018.Nitrogen loading affects microbes, nitrifiers and denitrifiers attached to submerged macrophyte in constructed wetlands.Science of the Total Environment, 622-623:121-126,
Yang Y D, Zhao J, Jiang Y et al.2017.Response of bacteria harboring nirS and nirK genes to different N fertilization rates in an alkaline northern Chinese soil.European Journal of Soil Biology, 82:1-9,
You X Q, Xu N, Yang X et al.2021.Pollutants affect algae-bacteria interactions:a critical review.Environmental Pollution, 276:116723,
Yu H, Liu X Y, Yang C et al.2021.Co-symbiosis of arbuscular mycorrhizal fungi (AMF) and diazotrophs promote biological nitrogen fixation in mangrove ecosystems.Soil Biology and Biochemistry, 161:108382,
Zhang S H, Pang S, Wang P F et al.2016.Responses of bacterial community structure and denitrifying bacteria in biofilm to submerged macrophytes and nitrate.Scientific Reports, 6(1):36178,
Zhang Z Q, Chen H Z, Mu X Y et al.2020.Nitrate application decreased microbial biodiversity but stimulated denitrifiers in epiphytic biofilms on Ceratophyllum demersum.Journal of Environmental Management, 269:110814,
Zheng Y L, Hou L J, Liu M et al.2015.Diversity, abundance, and distribution of nirS-harboring denitrifiers in intertidal sediments of the Yangtze Estuary.Microbial Ecology, 70(1):30-40,
Zhong X Z, Zeng Y, Wang S P et al.2020.Insight into the microbiology of nitrogen cycle in the dairy manure composting process revealed by combining high-throughput sequencing and quantitative PCR.Bioresource Technology, 301:122760,
Zhou J Z, Ning D L.2017.Stochastic community assembly:does it matter in microbial ecology? Microbiology and Molecular Biology Reviews, 81(4):e00002-17,
Zhou S L, Huang T L, Zhang C H et al.2016.Illumina MiSeq sequencing reveals the community composition of NirS-Type and NirK-Type denitrifiers in Zhoucun reservoir-A large shallow eutrophic reservoir in northern China.RSC Advances, 6(94):91517-91528,
Zhu J M, Zhou J, Wang H et al.2021.The ecological network approach to algal-bacterial relationships:review and prospects.Chinese Science Bulletin, 66(34):4378-4394,

Related Articles:
1.Guoqing LI, Dingbo YAN, Pinhua XIA, Haipeng CAO, Tao LIN, Yin YI.Community structure and assembly of denitrifying bacteria in epiphytic biofilms in a freshwater lake ecosystem[J]. Journal of Oceanology and Limnology, 2022,40(3): 1039-1050
Copyright © Haiyang Xuebao