Abstract
Extreme climatic activities, such as typhoons, are widely known to disrupt our natural environment. In particular, studies have revealed that typhoon-induced perturbations can result in several long-term effects on various ecosystems. In this study, we have conducted a 2-year metagenomic survey to investigate the microbial and viral community dynamics associated with environmental changes and seasonal variations in an enclosed freshwater reservoir subject to episodic typhoons. We found that the microbial community structure and the associated metagenomes continuously changed, where microbial richness increased after typhoon events and decreased during winter. Among the environmental factors that influenced changes in the microbial community, precipitation was considered to be the most significant. Similarly, the viral community regularly showed higher relative abundances and diversity during summer in comparison to winter, with major variations happening in several viral families including Siphoviridae, Myoviridae, Podoviridae and Microviridae. Interestingly, we also found that the precipitation level was associated with the terrestrial viral abundance in the reservoir. In contrast to the dynamic microbial community (L-divergence 0.73±0.25), we found that microbial metabolic profiles were relatively less divergent (L-divergence 0.24±0.04) at the finest metabolic resolution. This study provides for the first time a glimpse at the microbial and viral community dynamics of a subtropical freshwater ecosystem, adding a comprehensive set of new knowledge to aquatic environments.
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Angly FE, Felts B, Breitbart M, Salamon P, Edwards RA, Carlson C et al (2006). The marine viromes of four oceanic regions. PLoS Biol 4: e368.
Berg KA, Lyra C, Sivonen K, Paulin L, Suomalainen S, Tuomi P et al (2009). High diversity of cultivable heterotrophic bacteria in association with cyanobacterial water blooms. ISME J 3: 314–325.
Bolhuis H, Stal LJ . (2011). Analysis of bacterial and archaeal diversity in coastal microbial mats using massive parallel 16S rRNA gene tag sequencing. ISME J 5: 1701–1712.
Breitbart M . (2012). Marine viruses: truth or dare. Ann Rev Mar Sci 4: 425–448.
Burke C, Steinberg P, Rusch D, Kjelleberg S, Thomas T . (2011). Bacterial community assembly based on functional genes rather than species. Proc Natl Acad Sci USA 108: 14288–14293.
Byju P, Kumar SP . (2011). Physical and biological response of the Arabian Sea to tropical cyclone Phyan and its implications. Mar Environ Res 71: 325–330.
Chang J, Chung CC, Gong GC . (1996). Influences of cyclones on chlorophyll a concentration and Synechococcus abundance in a subtropical western Pacific coastal ecosystem. Mar Ecol Progr Ser 140: 199–205.
Chen CP, Tseng CH, Chen CA, Tang SL . (2011). The dynamics of microbial partnerships in the coral Isopora palifera. ISME J 5: 728–740.
Chen YJC, Wu SC, Lee BS, Hung CC . (2006). Behavior of storm-induced suspension interflow in subtropical Feitsui Reservoir, Taiwan. Limnol Oceanogr 51: 1125–1133.
Chenard C, Suttle CA . (2008). Phylogenetic diversity of sequences of cyanophage photosynthetic gene psbA in marine and freshwaters. Appl Environ Microbiol 74: 5317–5324.
DeLong EF, Karl DM . (2005). Genomic perspectives in microbial oceanography. Nature 437: 336–342.
Dinsdale EA, Edwards RA, Hall D, Angly F, Breitbart M, Brulc JM et al (2008). Functional metagenomic profiling of nine biomes. Nature 452: 629–632.
Djikeng A, Kuzmickas R, Anderson NG, Spiro DJ . (2009). Metagenomic analysis of RNA viruses in a fresh water lake. PLoS One 4: e7264.
Edwards RA, Rohwer F . (2005). Viral metagenomics. Nat Rev Microbiol 3: 504–510.
Fan CW, Kao SJ . (2008). Effects of climate events driven hydrodynamics on dissolved oxygen in a subtropical deep reservoir in Taiwan. Sci Tot Environ 393: 326–332.
Fancello L, Trape S, Robert C, Boyer M, Popgeorgiev N, Raoult D et al (2012). Viruses in the desert: a metagenomic survey of viral communities in four perennial ponds of the Mauritanian Sahara. ISME J 7: 359–369.
Gilbert JA, Steele JA, Caporaso JG, Steinbruck L, Reeder J, Temperton B et al (2012). Defining seasonal marine microbial community dynamics. ISME J 6: 298–308.
Grossart HP, Levold F, Allgaier M, Simon M, Brinkhoff T . (2005). Marine diatom species harbour distinct bacterial communities. Environ Microbiol 7: 860–873.
Hamady M, Lozupone C, Knight R . (2010). Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J 4: 17–27.
Hamp TJ, Jones WJ, Fodor AA . (2009). Effects of experimental choices and analysis noise on surveys of the ‘rare biosphere’. Appl Environ Microbiol 75: 3263–3270.
Hewson I, Poretsky RS, Tripp HJ, Montoya JP, Zehr JP . (2010). Spatial patterns and light-driven variation of microbial population gene expression in surface waters of the oligotrophic open ocean. Environ Microbiol 12: 1940–1956.
Hung CC, Gong GC . (2011). Biogeochemical responses in the Southern East China Sea after typhoons. Oceanography 24: 42–51.
Jardillier L, Zubkov MV, Pearman J, Scanlan DJ . (2010). Significant CO2 fixation by small prymnesiophytes in the subtropical and tropical northeast Atlantic Ocean. ISME J 4: 1180–1192.
Jones SE, Chiu CY, Kratz TK, Wu JT, Shade A, McMahon KD . (2008). Typhoons initiate predictable change in aquatic bacterial communities. Limnol Oceanogr 53: 1319–1326.
Kent WJ . (2002). BLAT—the BLAST-like alignment tool. Genome Res 12: 656–664.
Kim KH, Bae JW . (2011). Amplification methods bias metagenomic libraries of uncultured single-stranded and double-stranded DNA viruses. Appl Environ Microbiol 77: 7663–7668.
Kirchman DL . (2002). The ecology of Cytophaga–Flavobacteria in aquatic environments. FEMS Microbiol Ecol 39: 91–100.
Kristiansson E, Hugenholtz P, Dalevi D . (2009). ShotgunFunctionalizeR: an R-package for functional comparison of metagenomes. BioInformatics 25: 2737–2738.
Lin JH . (1991). Divergence measures based on the Shannon entropy. IEEE Trans Inform Theory 37: 145–151.
Lopez-Bueno A, Tamames J, Velazquez D, Moya A, Quesada A, Alcami A . (2009). High diversity of the viral community from an Antarctic Lake. Science 326: 858–861.
Marraffini LA, Sontheimer EJ . (2010). CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea. Nat Rev Genet 11: 181–190.
Ogawa H, Tanoue E . (2003). Dissolved organic matter in oceanic waters. J Oceanogr 59: 129–147.
Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH, Oksanen MJ et al (2007). The vegan package. Commun Ecol Package Version 1: 8–5.
Paerl HW, Valdes LM, Peierls BL, Adolf JE, Harding LW . (2006). Anthropogenic and climatic influences on the eutrophication of large estuarine ecosystems. Limnol Oceanogr 51: 448–462.
Partensky F, Hess WR, Vaulot D . (1999). Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 63: 106.
Paul JH, Sullivan MB . (2005). Marine phage genomics: what have we learned? Curr Opin Biotechnol 16: 299–307.
Powell S, Szklarczyk D, Trachana K, Roth A, Kuhn M, Muller J et al (2012). eggNOG v3.0: orthologous groups covering 1133 organisms at 41 different taxonomic ranges. Nucleic Acids Res 40: D284–D289.
Preiss J . (1984). Bacterial glycogen synthesis and its regulation. Annu Rev Microbiol 38: 419–458.
Rohwer F, Edwards R . (2002). The Phage Proteomic Tree: a genome-based taxonomy for phage. J Bacteriol 184: 4529–4535.
Roux S, Enault F, Robin A, Ravet V, Personnic S, Theil S et al (2012). Assessing the diversity and specificity of two freshwater viral communities through metagenomics. PLoS One 7: e33641.
Sanchez-Perez G, Mira A, Nyiro G, Pasic L, Rodriguez-Valera F . (2008). Adapting to environmental changes using specialized paralogs. Trends Genet 24: 154–158.
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB et al (2009). Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537–7541.
Shade A, Read JS, Welkie DG, Kratz TK, Wu CH, McMahon KD . (2011). Resistance, resilience and recovery: aquatic bacterial dynamics after water column disturbance. Environ Microbiol 13: 2752–2767.
Shade A, Read JS, Youngblut ND, Fierer N, Knight R, Kratz TK et al (2012). Lake microbial communities are resilient after a whole-ecosystem disturbance. ISME J 6: 2153–2167.
Shiah FK, Chung SW, Kao SJ, Gong GC, Liu KK . (2000). Biological and hydrographical responses to tropical cyclones (typhoons) in the continental shelf of the Taiwan Strait. Cont Shelf Res 20: 2029–2044.
Sousa WP . (1984). The role of disturbance in natural communities. Annu Rev Ecol System 15: 353–391.
Sullivan MB, Lindell D, Lee JA, Thompson LR, Bielawski JP, Chisholm SW . (2006). Prevalence and evolution of core photosystem II genes in marine cyanobacterial viruses and their hosts. PLoS Biol 4: e234.
Thurber RV, Haynes M, Breitbart M, Wegley L, Rohwer F . (2009). Laboratory procedures to generate viral metagenomes. Nat Protoc 4: 470–483.
Tseng YF, Hsu TC, Chen YL, Kao SJ, Wu JT, Lu JC et al (2010). Typhoon effects on DOC dynamics in a phosphate-limited reservoir. Aquat Microb Ecol 60: 247–260.
Vinayachandran PN, Mathew S . (2003). Phytoplankton bloom in the Bay of Bengal during the northeast monsoon and its intensification by cyclones. Geophys Res Lett 30: doi:10.1029/2002gl016717.
Walker ND, Leben RR, Balasubramanian S . (2005). Hurricane-forced upwelling and chlorophyll a enhancement within cold-core cyclones in the Gulf of Mexico. Geophys Res Lett 32: doi:10.1029/2005gl023716.
Wang Q, Garrity GM, Tiedje JM, Cole JR . (2007). Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73: 5261–5267.
Waterbury JB, Watson SW, Valois FW, Franks DG . (1986). Biological and ecological characterization of the marine unicellular cyano bacterium Synechococcus. Can J Fish Aquat Sci 214: 71–120.
West AJ, Lin CW, Lin TC, Hilton RG, Liu SH, Chang CT et al (2011). Mobilization and transport of coarse woody debris to the oceans triggered by an extreme tropical storm. Limnol Oceanogr 56: 77–85.
Wiedenbeck J, Cohan FM . (2011). Origins of bacterial diversity through horizontal genetic transfer and adaptation to new ecological niches. FEMS Microbiol Rev 35: 957–976.
Wilson K . (2001). Preparation of genomic DNA from bacteria. Curr Protoc Mol Biol Chapter 2: Unit 2.4; doi:10.1002/0471142727.mb0204s56.
Wu CC, Kuo YH . (1999). Typhoons affecting Taiwan: current understanding and future challenges. Bull Am Meteorol Soc 80: 67–80.
Wu XA, Monchy S, Taghavi S, Zhu W, Ramos J, van der Lelie D . (2011). Comparative genomics and functional analysis of niche-specific adaptation in Pseudomonas putida. FEMS Microbiol Rev 35: 299–323.
Zehetner F, Vemuri NL, Huh CA, Kao SJ, Hsu SC, Huang JC et al (2008). Soil and phosphorus redistribution along a steep tea plantation in the Feitsui reservoir catchment of northern Taiwan. Soil Sci Plant Nutr 54: 618–626.
Acknowledgements
We thank Taipei FTR Administration Bureau for their help in sample collection. This research was supported by the National Science Council (NSC) in Taiwan through Grant NSC 97-2621-B-001-004-MY2 and the NSC T-WEBS project. CHT was supported in part by the Student Exchange Program of National Yang-Ming University, and Australian Research Council (Grant Number DP1096296).
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Tseng, CH., Chiang, PW., Shiah, FK. et al. Microbial and viral metagenomes of a subtropical freshwater reservoir subject to climatic disturbances. ISME J 7, 2374–2386 (2013). https://doi.org/10.1038/ismej.2013.118
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DOI: https://doi.org/10.1038/ismej.2013.118
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