Effects of alternate drying-wetting cycles on biofilm characteristics and their microbial communities
LI Chun-yan1,2, XIE Shan-shan1,2, WANG Wen-wen1,2, ZHU Shi-jun1,2, WEN Chen1,2, LI Ni-hong1,2, LUO Xia1,2
1. Institute of International Rivers and Eco-Security, Yunnan University, Kunming 650500, China; 2. Yunnan Key Laboratory of International Rivers and Transboundary Eco-Security, Kunming 650500, China
Abstract:The periphytic biofilm was sampled in natural environment and cultivated under indoor controlled conditions to clarify the biofilm resistance mechanisms under the influence of alternate drying and wetting cycles. The morphology, microbial community structure, diversity and function of natural biofilms were examined using 16S rRNA gene high throughput sequencing and confocal laser scanning microscopy. The results showed that biofilm thickness was reduced from 9.10 to 6.46 μm with the increase of alternate drying-wetting cycles from one (C1) to five (C5). The extracellular polymer content decreased from 2.64 μm3/μm3 (control) to 1.9 μm3/μm3(C1), and then increased from 4.41 μm3/μm3(C3) to 1.54 μm3/μm3(C5, P=0.004). The ratio of live/dead bacteria increased from 2.52 (C1) to 3.60 (C3), and then decreased to 0.72(C5, P=0.009). However, the changes in surface area to volume ration and roughness coefficient with the alternate drying and wetting cycles were not significant compared to the control. In contrast to the control, the richness and diversity of the microbial community decreased and the indicator species changed when biofilm exposed to alternate drying and wetting cycles. The dominant bacteria in biofilm shifted from Proteobacteria to Cyanobacteria-related flora when the alternate drying and wetting cycles reached to five (C5). Moreover, functional groups associated with photoautotrophy became the most abundant. Therefore, biofilm morphology and microbial community structure were associated with the alternate drying and wetting cycles. Microbial communities exhibited high degrees of resistance under lower alternate drying and wetting cycles, whereas showed high degrees of resilience to increased alternate drying and wetting cycles.
李春艳, 谢珊珊, 王文文, 朱时俊, 闻晨, 李妮鸿, 骆霞. 干湿交替循环频率对生物膜特征及其微生物群落的影响[J]. 中国环境科学, 2023, 43(2): 854-862.
LI Chun-yan, XIE Shan-shan, WANG Wen-wen, ZHU Shi-jun, WEN Chen, LI Ni-hong, LUO Xia. Effects of alternate drying-wetting cycles on biofilm characteristics and their microbial communities. CHINA ENVIRONMENTAL SCIENCECE, 2023, 43(2): 854-862.
Datry T, Larned S T, Tockner K. Intermittent Rivers: A challenge for freshwater ecology [J]. Bioscience, 2014,64(3):229-235.
[2]
Corti R, Datry T. Terrestrial and aquatic invertebrates in the riverbed of an intermittent river: parallels and contrasts in community organisation [J]. Freshwater Biology, 2016,61(8):1308-1320.
[3]
Datry T, Fritz K, Leigh C. Challenges, developments and perspectives in intermittent river ecology [J]. Freshwater Biology. 2016,61(8): 1171-1180.
[4]
Ylla I, Sanpera-Calbet I, Vazquez E, et al. Organic matter availability during pre-and post-drought periods in a Mediterranean stream [J]. Hdrobiologia, 2010,657(1):217-232.
[5]
Fazi S, Vazquez E, Casamayor E O, et al. Stream hydrological fragmentation drives bacterioplankton community composition [J]. Plos One, 2013,8(5):0064109.
[6]
Tzoraki O, Nikolaidis N P, Amaxidis Y, et al. In-stream biogeochemical processes of a temporary river [J]. Environmental Science & Technology, 2007,41(4):1225-1231.
[7]
Barthès A, Ten-Hage L, Lamy A, et al. Resilience of aggregated microbial communities subjected to drought—small-scale studies [J]. Microbial Ecology, 2015,70(1):9-20.
[8]
Flemming H, Wingender J. The biofilm matrix [J]. Nature Reviews Microbiology, 2010,8(9):623-633.
[9]
Weaver L, Webber J B, Hickson A C, et al. Biofilm resilience to desiccation in groundwater aquifers: a laboratory and field study [J]. Science of The Total Environment, 2015,514:281-289.
[10]
周新,张伟,崔 鸿.生态系统的抵抗力和恢复力稳定性 [J]. 生物学教学, 2014,39(4):4-5. Zhou X, Zhou W, Cui H, et al. Resistance and resilience stability of ecosystem [J]. Biology Teaching, 2014,39(4):4-5.
[11]
何红英.对"生态系统抵抗力稳定性和恢复力稳定性"的辨析 [J]. 中学生物学, 2013,29(3):3-4. He H Y. Analysis of "Ecosystem resistance and resilience stability" [J]. Middle School Biology, 2013,29(3):3-4.
[12]
李超然,苗令占,侯 俊.间歇性河流中生物膜对干湿胁迫的动态响应 [J]. 中国环境科学, 2021,41(11):5245-5253. Li C R, Miao L Z, Hou J, et al. Dynamic response of biofilm to dry and wet stress in intermittent rivers [J]. China Environmental Science, 2021,41(11):5245-5253.
[13]
Mckew B A, Taylor J D, Mcgenity T J, et al. Resistance and resilience of benthic biofilm communities from a temperate saltmarsh to desiccation and rewetting [J]. ISME J, 2011,5(1):30-41.
[14]
Febria C M, Beddoes P, Fulthorpe R R, et al. Bacterial community dynamics in the hyporheic zone of an intermittent stream [J]. ISME J, 2012,6(5):1078-1088.
[15]
Timoner X, Acuna V, Frampton L, et al. Biofilm functional responses to the rehydration of a dry intermittent stream [J]. Hydrobiologia, 2014,727(1):185-195.
[16]
宋云龙,张金松,朱 佳,等.基于高通量测序的微生物强化污泥减量工艺中微生物群落解析 [J]. 中国环境科学, 2016,(7):2099-2107. Song Y L, Zhang J S, Zhu J, et al. Analysis of microbial community in microbial enhanced sludge reduction process based on high-throughput sequencing [J]. China Environmental Science, 2016,(7): 2099-2107.
[17]
Zlatanović S, Fabian J, Premke K, et al. Shading and sediment structure effects on stream metabolism resistance and resilience to infrequent droughts [J]. Science of The Total Environment, 2018, 621:1233-1242.
[18]
Acuña V, Casellas M, Corcoll N, et al. Increasing extent of periods of no flow in intermittent waterways promotes heterotrophy [J]. Freshwater Biology, 2015,60(9):1810-1823.
[19]
Luo X, Yang Y H, Xie S S, et al. Drying and rewetting induce changes in biofilm characteristics and the release of metal ions [J]. Journal of Hazardous Materials, 2022,433:128832.
[20]
Romaní A M, Vázquez E, Butturini A. Microbial availability and size fractionation of dissolved organic carbon after drought in an intermittent stream: biogeochemical link across the stream–riparian interface [J]. Microbial Ecology, 2006,52(3):501-512.
[21]
Mckew B A, Taylor J D, Mcgenity T J, et al. Resistance and resilience of benthic biofilm communities from a temperate saltmarsh to desiccation and rewetting [J]. The ISME Journal, 2011,5(1):30-41.
[22]
Gonzalez A G, Mombo S, Leflaive J, et al. Silver nanoparticles impact phototrophic biofilm communities to a considerably higher degree than ionic silver [J]. Environmental Science and Pollution Research, 2015,22(11):8412-8424.
[23]
Luo X, Xiang X Y, Huang G Y, et al. Bacterial abundance and physicochemical characteristics of water and sediment associated with hydroelectric dam on the Lancang River China [J]. International Journal of Environmental Research and Public Health, 2019,16(11):2031.
[24]
Luo X, Jedlicka S, Jellison K. Pseudo-second-order calcium-Mediated Cryptosporidium parvum oocyst attachment to environmental biofilms [J]. Appled and Environmental Microbiology, 2017,83(1):02339-16.
[25]
Luo X, Jedlicka S S, Jellison K L. Role of wall shear stress in Cryptosporidium parvum oocyst attachment to environmental biofilms [J]. Appled and Environmental Microbiology, 2017,83(24):01533-17.
[26]
Wunder D B, Bosscher V A, Cok R C, et al. Sorption of antibiotics to biofilm [J]. Water Research, 2011,45(6):2270-2280.
[27]
Luo X, Jellison K L, Huynh K, et al. Impact of bioreactor environment and recovery method on the profile of bacterial populations from water distribution systems [J]. Plos One, 2015,10(7):e0133427.
[28]
Garny K, Neu T R, Horn H, et al. Combined application of C-13NMR spectroscopy and confocal laser scanning microscopy-Investigation on biofilm structure and physico-chemical properties [J]. Chemical Engineering Science, 2010,65(16):4691-4700.
[29]
Neu T R, Woelfl S, Lawrence J R. Three-dimensional differentiation of photo-autotrophic biofilm constituents by multi-channel laser scanning microscopy (single-photon and two-photon excitation) [J]. Journal of Microbiological Methods, 2004,56(2):161-172.
[30]
Heydorn A, Nielsen A T, Hentzer M, et al. Quantification of biofilm structures by the novel computer program Comstat [J]. Microbiology-SGM, 2000,146:2395-2407.
[31]
Onay E O, Alikaya C, Seker E. Evaluation of antifungal efficacy of erbium, chromium: Yttrium-Scandium-Gallium-Garnet laser against Candida albicans [J]. Photomedicine and Laser Surgery, 2010, 28:S73-S78.
[32]
Edgar R C. UPARSE: highly accurate OTU sequences from microbial amplicon reads [J]. Nature Methods, 2013,10(10):996.
[33]
Caporaso J G, Kuczynski J, Stombaugh J, et al. QIIME allows analysis of high-throughput community sequencing data [J]. Nature Methods, 2010,7(5):335-336.
[34]
Pruesse E, Quast C, Knittel K, et al. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB [J]. Nucleic Acids Research, 2007,35(21): 7188-7196.
[35]
Wickham H, Chang W. ggplot2: an implementation of the grammar of graphics [J]. R package version 0.7, URL: http://CRAN.R-project.org/package=ggplot2,2008,3.
[36]
Oksanen J, Blanchet FG, Kindt R, et al. Vegan: community ecology package [M]. R package version 1.17-4, URL: http://cran.r-project.org>.Acessoem,2010,23:2010.
[37]
Roberts D. labdsv: Ordination and Multivariate Analysis for Ecology [M]//2013.
[38]
Louca S, Parfrey L W, Doebeli M. Decoupling function and taxonomy in the global ocean microbiome [J]. Science, 2016,353(6305):1272-1277.
[39]
Naseem H, Ahsan M, Shahid M A, et al. Exopolysaccharides producing rhizobacteria and their role in plant growth and drought tolerance [J]. Journal of Basic Microbiology, 2018,58(12):1009-1022.
[40]
Zhou H, Sheng Y, Zhao X, et al. Treatment of acidic sulfate-containing wastewater using revolving algae biofilm reactors: Sulfur removal performance and microbial community characterization [J]. Bioresource Technology, 2018,264:24-34.
[41]
Schimel J, Balser T C, Wallenstein M. Microbial stress-response physiology and its implications for ecosystem function [J]. Ecology, 2007,88(6):1386-1394.
[42]
Ustunturk-Onan M, Hoca S, Ilhan-Sungur E. The Effect of Short-Term Drying on Biofilm Formed in a Model Water Distribution System [J]. Microbiology, 2018,87(6):857-864.
[43]
Amalfitano S, Fazi S, Zoppini A, et al. Responses of benthic bacteria to experimental drying in sediments from Mediterranean temporary rivers [J]. Microbial Ecology, 2008,55(2):270-279.
[44]
Bu X, Gu X, Zhou X, et al. Extreme drought slightly decreased soil labile organic C and N contents and altered microbial community structure in a subtropical evergreen forest [J]. Forest Ecology and Management, 2018,429:18-27.
[45]
Fuentes E, Prieto B. Recovery capacity of subaerial biofilms grown on granite buildings subjected to simulated drought in a climate change context [J]. Microbial Ecology, 2021,82(3):761-769.
[46]
黄兴,孙宝盛,孙井梅,等.贫营养条件下EPS、SMP和微生物多样性的研究 [J]. 环境科学, 2009,30(5):1468-1474. Huang X, Sun B S, Sun J M, et al. EPS, SMP and Microbial Biodiversity Under the Oligotrophic Environment [J]. Environmental Science, 2009,30(5):1468-1474.
[47]
Guo Y, Peng Y, Wang B, et al. Achieving simultaneous nitrogen removal of low C/N wastewater and external sludge reutilization in a sequencing batch reactor [J]. Chemical Engineering Journal, 2020, 306:925-932.
[48]
Santos F, Pena A, Nogales B, et al. Bacterial diversity in dry modern freshwater stromatolites from Ruidera Pools Natural Park, Spain [J]. Systematic and Applied Microbiology, 2010,33(4):209-221.
[49]
李军,张翠云,蓝芙宁,等.区域地下水不同深度微生物群落结构特征 [J]. 中国环境科学, 2019,(6):2614-2623. Li J, Zhang C Y, Lan F N, et al. Characteristics of microbial community structure in different depths of regional groundwater [J]. China Environmental Science, 2019,(6):2614-2623.
[50]
金梦婷,朱 亮,朱 彧,等.城市缓流水体生物膜群落与环境因子响应关系 [J]. 湖泊科学, 2015,27(1):58-66. Jin M T, Zhu L, Zhu Y, et al. Relationship between biofilm community and environmental factors in urban slow-flow water [J]. Journal of Lake Sciences, 2015,27(1):58-66.
[51]
Battin T J, Besemer K, Bengtsson M M, et al. The ecology and biogeochemistry of stream biofilms [J]. Nature Reviews Microbiology, 2016,14(4):251-263.
[52]
Or D, Phutane S, Dechesne A. Extracellular polymeric substances affecting pore-Scale hydrologic conditions for bacterial activity in unsaturated soils [J]. Vadose Zone Journal, 2007,6(2):298-305.
[53]
Romaní A M, Amalfitano S, Artigas J, et al. Microbial biofilm structure and organic matter use in mediterranean streams [J]. Hydrobiologia, 2013,719(1):43-58.
[54]
Sabater S, Timoner X, Bornette G, et al. The Biota of intermittent rivers andephemeral streams: algae and vascular plants [J]. Intermittent Rivers and Ephemeral Streams, 2017:189-216.
[55]
Marxsen J, Zoppini A, Wilczek S. Microbial communities in streambed sediments recovering from desiccation [J]. FEMS Microbiology Ecology, 2010,71(3):374-386.