Abstract
High-throughput sequencing (HTS) was used to analyze the seasonal variations in the bacterioplankton community composition (BCC) in the euphotic layer of a large and deep lake south of the Alps (Lake Garda). The BCC was analyzed throughout two annual cycles by monthly samplings using the amplification and sequencing of the V3–V4 hypervariable region of the 16S rRNA gene by the MiSeq Illumina platform. The dominant and most diverse bacterioplankton phyla were among the more frequently reported in freshwater ecosystems, including the Proteobacteria, Cyanobacteria, Bacteroidetes, Verrucomicrobia, Actinobacteria, and Planctomycetes. As a distinctive feature, the development of the BCC showed a cyclical temporal pattern in the two analyzed years and throughout the euphotic layer. The recurring temporal development was controlled by the strong seasonality in water temperature and thermal stratification, and by cyclical temporal changes in nutrients and, possibly, by the remarkable annual cyclical development of cyanobacteria and eukaryotic phytoplankton hosting bacterioplankton that characterizes Lake Garda. Further downstream analyses of operational taxonomic units associated to cyanobacteria allowed confirming the presence of the most abundant taxa previously identified by microscopy and/or phylogenetic analyses, as well as the presence of other small Synechococcales/Chroococcales and rare Nostocales never identified so far in the deep lakes south of the Alps. The implications of the high diversity and strong seasonality are relevant, opening perspectives for the definition of common and discriminating patterns characterizing the temporal and spatial distribution in the BCC, and for the application of the new sequencing technologies in the monitoring of water quality in large and deep lakes.
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Falkowski PG, Fenchel T, Delong EF (2008) The microbial engines that drive Earth’s biogeochemical cycles. Science (New York, NY) 320:1034–1039. https://doi.org/10.1126/science.1153213
Fenchel T (2008) The microbial loop—25 years later. J Exp Mar Biol Ecol 366:99–103. https://doi.org/10.1016/j.jembe.2008.07.013
Weisse T (2004) Pelagic microbes—protozoa and the microbial food web. In: O’Sullivan PE, Reynolds CS (eds) The lakes handbook. Volume 1. Limnology and limnetic ecology. Blackwell Publishing, Malden, pp 417–460
De Wever A, Muylaert K, Van der Gucht K et al (2005) Bacterial community composition in Lake Tanganyika: vertical and horizontal heterogeneity. Appl. Environ. Microbiol. 71:5029–5037. https://doi.org/10.1128/AEM.71.9.5029-5037.2005
Plasencia A, Gich F, Fillol M, Borrego CM (2013) Phylogenetic characterization and quantification of ammonia-oxidizing archaea and bacteria from Lake Kivu in a long-term microcosm incubation. Int Microbiol 16:177–189. https://doi.org/10.2436/20.1501.01.192
Brown JW (2015) Principles of microbial diversity. https://doi.org/10.1128/9781555818517
Pessi IS, Maalouf PDC, Laughinghouse HD et al (2016) On the use of high-throughput sequencing for the study of cyanobacterial diversity in Antarctic aquatic mats. J Phycol 52:356–368. https://doi.org/10.1111/jpy.12399
Tytgat B, Verleyen E, Obbels D et al (2014) Bacterial diversity assessment in antarctic terrestrial and aquatic microbial mats: a comparison between bidirectional pyrosequencing and cultivation. PLoS One 9:e97564. https://doi.org/10.1371/journal.pone.0097564
Venter JC, Remington K, Heidelberg JF et al (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science (New York, NY) 304:66–74. https://doi.org/10.1126/science.1093857
Sunagawa S, Coelho LP, Chaffron S et al (2015) Ocean plankton. Structure and function of the global ocean microbiome. Science (New York, N.Y.) 348:1261359. https://doi.org/10.1126/science.1261359
Tringe SG, Hugenholtz P (2008) A renaissance for the pioneering 16S rRNA gene. Curr. Opin. Microbiol. 11:442–446. https://doi.org/10.1016/j.mib.2008.09.011
Oulas A, Pavloudi C, Polymenakou P et al (2015) Metagenomics: tools and insights for analyzing next-generation sequencing data derived from biodiversity studies. Bioinf Biol Insights 9:75–88. https://doi.org/10.4137/BBI.S12462
Tammert H, Tšertova N, Kiprovskaja J et al (2015) Contrasting seasonal and interannual environmental drivers in bacterial communities within a large shallow lake: evidence from a seven year survey. Aquat. Microb. Ecol. 75:43–54. https://doi.org/10.3354/ame01744
Beall BFN, Twiss MR, Smith DE et al (2016) Ice cover extent drives phytoplankton and bacterial community structure in a large north-temperate lake: implications for a warming climate. Environ. Microbiol. 18:1704–1719. https://doi.org/10.1111/1462-2920.12819
Salmaso N, Mosello R (2010) Limnological research in the deep southern subalpine lakes: synthesis, directions and perspectives. Adv. Oceanogr. Limnol. 1:29–66. https://doi.org/10.1080/19475721003735773
Bertoni R, Callieri C, Corno G et al (2010) Long-term trends of epilimnetic and hypolimnetic bacteria and organic carbon in a deep holo-oligomictic lake. Hydrobiologia 644:279–287. https://doi.org/10.1007/s10750-010-0150-x
Callieri C, Cronberg G, Stockner JG (2012) Freshwater picocyanobacteria: single cells, microcolonies and colonial forms. Springer, Netherlands, pp 229–269
Callieri C, Amalfitano S, Corno G, Bertoni R (2016) Grazing-induced Synechococcus microcolony formation: experimental insights from two freshwater phylotypes. FEMS Microbiol Ecol 92:fiw154. https://doi.org/10.1093/femsec/iw154
Coci M, Odermatt N, Salcher MM, et al (2015) Ecology and distribution of Thaumarchaea in the deep hypolimnion of Lake Maggiore. Archaea 2015/59043:11 pp. https://doi.org/10.1155/2015/590434
Callieri C, Hernández-Avilés S, Salcher MM et al (2016) Distribution patterns and environmental correlates of Thaumarchaeota abundance in six deep subalpine lakes. Aquat. Sci. 78:215–225. https://doi.org/10.1007/s00027-015-0418-3
Salmaso N, Morabito G, Mosello R et al (2003) A synoptic study of phytoplankton in the deep lakes south of the Alps (lakes Garda, Iseo, Como, Lugano and Maggiore). J. Limnol. 62:207. https://doi.org/10.4081/jlimnol.2003.207
Salmaso N, Padisák J (2007) Morpho-functional groups and phytoplankton development in two deep lakes (Lake Garda, Italy and Lake Stechlin, Germany). Hydrobiologia 578:97–112. https://doi.org/10.1007/s10750-006-0437-0
Salmaso N (2011) Interactions between nutrient availability and climatic fluctuations as determinants of the long-term phytoplankton community changes in Lake Garda, Northern Italy. Hydrobiologia 660:59–68. https://doi.org/10.1007/s10750-010-0394-5
Meriluoto J, Blaha L, Bojadzija G et al (2017) Toxic cyanobacteria and cyanotoxins in European waters – recent progress achieved through the CYANOCOST. Action and challenges for further research. Adv Oceanogr Limnol 8:161–178. https://doi.org/10.4081/aiol.2017.6429
Savela H, Spoof L, Perälä N et al (2017) First report of cyanobacterial paralytic shellfish toxin biosynthesis genes and paralytic shellfish toxin production in Polish freshwater lakes. Adv Oceanogr Limnol 8:61–70. https://doi.org/10.4081/aiol.2017.6319
Sukenik A, Quesada A, Salmaso N (2015) Global expansion of toxic and non-toxic cyanobacteria: effect on ecosystem functioning. Biodivers Conserv 24:889–908. https://doi.org/10.1007/s10531-015-0905-9
Shams S, Capelli C, Cerasino L et al (2015) Anatoxin-a producing Tychonema (Cyanobacteria) in European waterbodies. Water Res. 69:68–79. https://doi.org/10.1016/j.watres.2014.11.006
Salmaso N, Cerasino L (2012) Long-term trends and fine year-to-year tuning of phytoplankton in large lakes are ruled by eutrophication and atmospheric modes of variability. Hydrobiologia 698:17–28. https://doi.org/10.1007/s10750-012-1068-2
Read JS, Hamilton DP, Jones ID et al (2011) Derivation of lake mixing and stratification indices from high-resolution lake buoy data. Environ. Model Softw. 26:1325–1336. https://doi.org/10.1016/j.envsoft.2011.05.006
Cerasino L, Salmaso N (2012) Diversity and distribution of cyanobacterial toxins in the Italian subalpine lacustrine district. Oceanol. Hydrobiol. Stud. 41:54–63. https://doi.org/10.2478/s13545-012-0028-9
R Core Team (2017) R: A language and environment for statistical computing (v. 3.4.1). R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/
Yuan S, Cohen DB, Ravel J et al (2012) Evaluation of methods for the extraction and purification of DNA from the human microbiome. PLoS One 7:e33865. https://doi.org/10.1371/journal.pone.0033865
Bag S, Saha B, Mehta O et al (2016) An improved method for high quality metagenomics DNA extraction from human and environmental samples. Sci. Rep. 6:26775. https://doi.org/10.1038/srep26775
Herlemann DP, Labrenz M, Jürgens K et al (2011) Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J 5:1571–1579. https://doi.org/10.1038/ismej.2011.41
Klindworth A, Pruesse E, Schweer T et al (2013) Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 41:e1. https://doi.org/10.1093/nar/gks808
Apprill A, McNally S, Parsons R, Weber L (2015) Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton. Aquat. Microb. Ecol. 75:129–137
Albanese D, Fontana P, De Filippo C et al (2015) MICCA: a complete and accurate software for taxonomic profiling of metagenomic data. Sci. Rep. 5:9743. https://doi.org/10.1038/srep09743
Quast C, Pruesse E, Yilmaz P et al (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41:D590–D596. https://doi.org/10.1093/nar/gks1219
Rognes T, Flouri T, Nichols B et al (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ 4:e2584. https://doi.org/10.7717/peerj.2584
DeSantis TZ, Hugenholtz P, Keller K et al (2006) NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes. Nucleic Acids Res. 34:W394–W399. https://doi.org/10.1093/nar/gkl244
Price MN, Dehal PS, Arkin AP (2010) FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS One 5:e9490. https://doi.org/10.1371/journal.pone.0009490
McMurdie PJ, Holmes S (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8:e61217. https://doi.org/10.1371/journal.pone.0061217
Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 71:8228–8235. https://doi.org/10.1128/AEM.71.12.8228-8235.2005
Legendre P, Gallagher E (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280. https://doi.org/10.1007/s004420100716
Legendre P, Legendre L (1998) Numerical ecology, Second Eng. Elsevier Science BV, Amsterdam
Jackson DA (1995) PROTEST: a PROcrustean randomization TEST of community environment concordance. Écoscience 2:297–303. https://doi.org/10.1080/11956860.1995.11682297
Oksanen J, Blanchet FG, Friendly M, et al (2016) vegan: Community Ecology Package. 285
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x
Flores GE, Bates ST, Knights D et al (2011) Microbial biogeography of public restroom surfaces. PLoS One 6:e28132. https://doi.org/10.1371/journal.pone.0028132
Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York
Garnier S (2017) Viridis: default color maps from “matplotlib”. R package version 0.4.0
Yoon S-H, Ha S-M, Kwon S et al (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA and whole genome assemblies. Int. J. Syst. Evol. Microbiol. https://doi.org/10.1099/ijsem.0.001755
Cole JR, Wang Q, Fish JA et al (2014) Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res. 42:D633–D642. https://doi.org/10.1093/nar/gkt1244
Eren AM, Maignien L, Sul WJ et al (2013) Oligotyping: differentiating between closely related microbial taxa using 16S rRNA gene data. Methods Ecol. Evol. 4:1111–1119. https://doi.org/10.1111/2041-210X.12114
Fisher JC, Levican A, Figueras MJ, McLellan SL (2014) Population dynamics and ecology of Arcobacter in sewage. Front. Microbiol. 5:525. https://doi.org/10.3389/fmicb.2014.00525
Berry MA, White JD, Davis TW et al (2017) Are oligotypes meaningful ecological and phylogenetic units? A case study of Microcystis in freshwater lakes. Front. Microbiol. 8:365. https://doi.org/10.3389/fmicb.2017.00365
Eren AM, Morrison HG, Lescault PJ et al (2015) Minimum entropy decomposition: unsupervised oligotyping for sensitive partitioning of high-throughput marker gene sequences. ISME J 9:968–979. https://doi.org/10.1038/ismej.2014.195
Ercolini D (2013) High-throughput sequencing and metagenomics: moving forward in the culture-independent analysis of food microbial ecology. Appl. Environ. Microbiol. 79:3148–3155. https://doi.org/10.1128/AEM.00256-13
Boone DR, Castenholz RW (2001) Bergey’s manual of systematic bacteriology. Volume one—the archaea and the deeply branching and phototrophic bacteria. Springer Verlag, New York
Salmaso N, Capelli C, Shams S, Cerasino L (2015) Expansion of bloom-forming Dolichospermum lemmermannii (Nostocales, Cyanobacteria) to the deep lakes south of the Alps: colonization patterns, driving forces and implications for water use. Harmful Algae 50:76–87. https://doi.org/10.1016/j.hal.2015.09.008
Salmaso N, Cerasino L, Boscaini A, Capelli C (2016) Planktic Tychonema (Cyanobacteria) in the large lakes south of the Alps: phylogenetic assessment and toxigenic potential. FEMS Microbiol. Ecol. https://doi.org/10.1093/femsec/fiw155
Capelli C, Ballot A, Cerasino L et al (2017) Biogeography of bloom-forming microcystin producing and non-toxigenic populations of Dolichospermum lemmermannii (Cyanobacteria). Harmful Algae 67:1–12. https://doi.org/10.1016/j.hal.2017.05.004
Rieck A, Herlemann DPR, Jürgens K, Grossart H-P (2015) Particle-associated differ from free-living bacteria in surface waters of the Baltic Sea. Front. Microbiol. 6:1297. https://doi.org/10.3389/fmicb.2015.01297
Merkel AY, Korneeva VA, Tarnovetskii IY et al (2015) Structure of the archaeal community in the Black Sea photic zone. Microbiology 84:570–576. https://doi.org/10.1134/S0026261715040128
Milici M, Deng Z-L, Tomasch J et al (2016) Co-occurrence analysis of microbial taxa in the Atlantic Ocean reveals high connectivity in the free-living bacterioplankton. Front. Microbiol. 7:649. https://doi.org/10.3389/fmicb.2016.00649
Doherty M, Yager PL, Moran MA et al (2017) Bacterial biogeography across the Amazon River-ocean continuum. Front. Microbiol. 8:882. https://doi.org/10.3389/fmicb.2017.00882
Yang C, Wang Q, Simon PN et al (2017) Distinct network interactions in particle-associated and free-living bacterial communities during a Microcystis aeruginosa bloom in a plateau lake. Front. Microbiol. 8:1202. https://doi.org/10.3389/fmicb.2017.01202
Kurilkina MI, Zakharova YR, Galachyants YP et al (2016) Bacterial community composition in the water column of the deepest freshwater Lake Baikal as determined by next-generation sequencing. FEMS Microbiol. Ecol. 92:fiw094. https://doi.org/10.1093/femsec/fiw094
Llirós M, Inceoğlu Ö, García-Armisen T et al (2014) Bacterial community composition in three freshwater reservoirs of different alkalinity and trophic status. PLoS One 9:e116145. https://doi.org/10.1371/journal.pone.0116145
Kara EL, Hanson PC, Hu YH et al (2013) A decade of seasonal dynamics and co-occurrences within freshwater bacterioplankton communities from eutrophic Lake Mendota, WI, USA. ISME J 7:680–684. https://doi.org/10.1038/ismej.2012.118
Pollet T, Tadonleke RD, Humbert JF (2011) Spatiotemporal changes in the structure and composition of a less-abundant bacterial phylum (Planctomycetes) in two perialpine lakes. Appl. Environ. Microbiol. 77:4811–4821. https://doi.org/10.1128/AEM.02697-10
Pollet T, Humbert J-F, Tadonléké RD (2014) Planctomycetes in lakes: poor or strong competitors for phosphorus? Appl. Environ. Microbiol. 80:819–828. https://doi.org/10.1128/AEM.02824-13
Logue JB, Langenheder S, Andersson AF et al (2012) Freshwater bacterioplankton richness in oligotrophic lakes depends on nutrient availability rather than on species-area relationships. ISME J 6:1127–1136. https://doi.org/10.1038/ismej.2011.184
Walsby AE (2005) Stratification by cyanobacteria in lakes: a dynamic buoyancy model indicates size limitations met by Planktothrix rubescens filaments. New Phytol 168:365–376. https://doi.org/10.1111/j.1469-8137.2005.01508.x
Padisák J, Soróczki-Pintér É, Rezner Z (2003) Sinking properties of some phytoplankton shapes and the relation of form resistance to morphological diversity of plankton—an experimental study. Hydrobiologia 500:243–257. https://doi.org/10.1023/A:1024613001147
Kouzuma A, Watanabe K (2015) Exploring the potential of algae/bacteria interactions. Curr. Opin. Biotechnol. 33:125–129. https://doi.org/10.1016/j.copbio.2015.02.007
Ramanan R, Kim B-H, Cho D-H et al (2016) Algae–bacteria interactions: evolution, ecology and emerging applications. Biotechnol. Adv. 34:14–29. https://doi.org/10.1016/j.biotechadv.2015.12.003
Secker NH, Chua JPS, Laurie RE et al (2016) Characterization of the cyanobacteria and associated bacterial community from an ephemeral wetland in New Zealand. J. Phycol. 52:761–773. https://doi.org/10.1111/jpy.12434
Parveen B, Mary I, Vellet A et al (2013) Temporal dynamics and phylogenetic diversity of free-living and particle-associated Verrucomicrobia communities in relation to environmental variables in a mesotrophic lake. FEMS Microbiol. Ecol. 83:189–201. https://doi.org/10.1111/j.1574-6941.2012.01469.x
Seymour JR, Amin SA, Raina J-B, Stocker R (2017) Zooming in on the phycosphere: the ecological interface for phytoplankton–bacteria relationships. Nat Microbiol 2:17065. https://doi.org/10.1038/nmicrobiol.2017.65
Sigee DC (2005) Freshwater microbiology: biodiversity and dynamic interactions of microorganisms in the aquatic environment. J. Wiley
Friedman J, Alm EJ (2012) Inferring correlation networks from genomic survey data. PLoS Comput. Biol. 8:e1002687. https://doi.org/10.1371/journal.pcbi.1002687
Dorado-Morales P, Vilanova C, Garay PC et al (2016) Unveiling bacterial interactions through multidimensional scaling and dynamics modeling. Sci. Rep. 5:18396. https://doi.org/10.1038/srep18396
Newton RJ, Jones SE, Eiler A et al (2011) A guide to the natural history of freshwater lake bacteria. Microbiol Mol Biol Rev 75:14–49. https://doi.org/10.1128/MMBR.00028-10
Eiler A, Ollson JA, Bertillson S (2006) Diurnal variations in the auto- and heterotrophic activity of cyanobacterial phycospheres (Gloeotrichia echinulata) and the identity of attached bacteria. Freshw. Biol. 51:298–311. https://doi.org/10.1111/j.1365-2427.2005.01493.x
Hahn MW, Kasalický V, Jezbera J et al (2010) Limnohabitans curvus gen. nov., sp. nov., a planktonic bacterium isolated from a freshwater lake. Int. J. Syst. Evol. Microbiol. 60:1358–1365. https://doi.org/10.1099/ijs.0.013292-0
Hutalle-Schmelzer KML, Zwirnmann E, Krüger A, Grossart H-P (2010) Enrichment and cultivation of pelagic bacteria from a humic lake using phenol and humic matter additions. FEMS Microbiol. Ecol. 72:58–73. https://doi.org/10.1111/j.1574-6941.2009.00831.x
Corno G (2006) Effects of nutrient availability and Ochromonas sp. predation on size and composition of a simplified aquatic bacterial community. FEMS Microbiol. Ecol. 58:354–363. https://doi.org/10.1111/j.1574-6941.2006.00185.x
Salcher M, Pernthaler J, Psenner R, Posch T (2005) Succession of bacterial grazing defense mechanisms against protistan predators in an experimental microbial community. Aquat. Microb. Ecol. 38:215–229. https://doi.org/10.3354/ame038215
Brenner DJ, Krieg NR, Staley JT, Garrity GM (2005) Bergey’s manual of systematic bacteriology—volume two the Proteobacteria. Springer, Berlin
Eiler A, Bertilsson S (2004) Composition of freshwater bacterial communities associated with cyanobacterial blooms in four Swedish lakes. Environ. Microbiol. 6:1228–1243. https://doi.org/10.1111/j.1462-2920.2004.00657.x
Zeder M, Peter S, Shabarova T, Pernthaler J (2009) A small population of planktonic Flavobacteria with disproportionally high growth during the spring phytoplankton bloom in a prealpine lake. Environ. Microbiol. 11:2676–2686. https://doi.org/10.1111/j.1462-2920.2009.01994.x
Pernthaler J, Zollner E, Warnecke F, Jurgens K (2004) Bloom of filamentous bacteria in a mesotrophic lake: identity and potential controlling mechanism. Appl. Environ. Microbiol. 70:6272–6281. https://doi.org/10.1128/AEM.70.10.6272-6281.2004
Krieg NR, Staley JT, Brown DR, et al (2010) Bergey’s manual of systematic bacteriology, Vol. 4, 2nd Ed —The Bacteroidetes, Spirochaetes, Tenericutes (Mollicutes), Acidobacteria, Fibrobacteres, Fusobacteria, Dictyoglomi, Gemmatimonadetes, Lentisphaerae, Verrucomicrobia, Chlamydiae, Planctomycetes. https://doi.org/10.1007/978-0-387-68572-4
Eiler A, Bertilsson S (2007) Flavobacteria blooms in four eutrophic lakes: linking population dynamics of freshwater bacterioplankton to resource availability. Appl. Environ. Microbiol. 73:3511–3518. https://doi.org/10.1128/AEM.02534-06
J-H Q, Yuan H-L (2008) Sediminibacterium salmoneum gen. nov., sp. nov., a member of the phylum Bacteroidetes isolated from sediment of a eutrophic reservoir. Int. J. Syst. Evol. Microbiol. 58:2191–2194. https://doi.org/10.1099/ijs.0.65514-0
Kang H, Kim H, Lee B-I et al (2014) Sediminibacterium goheungense sp. nov., isolated from a freshwater reservoir. Int. J. Syst. Evol. Microbiol. 64:1328–1333. https://doi.org/10.1099/ijs.0.055137-0
Birtel J, Walser J-C, Pichon S et al (2015) Estimating bacterial diversity for ecological studies: methods, metrics, and assumptions. PLoS One 10:e0125356. https://doi.org/10.1371/journal.pone.0125356
Ávila MP, Staehr PA, Barbosa FAR et al (2017) Seasonality of freshwater bacterioplankton diversity in two tropical shallow lakes from the Brazilian Atlantic Forest. FEMS Microbiol. Ecol. 93:fiw218. https://doi.org/10.1093/femsec/fiw218
Chin KJ, Liesack W, Janssen PH (2001) Opitutus terrae gen. nov., sp. nov., to accommodate novel strains of the division “Verrucomicrobia” isolated from rice paddy soil. Int. J. Syst. Evol. Microbiol. 51:1965–1968. https://doi.org/10.1099/00207713-51-6-1965
Glöckner FO, Zaichikov E, Belkova N et al (2000) Comparative 16S rRNA analysis of lake bacterioplankton reveals globally distributed phylogenetic clusters including an abundant group of Actinobacteria. Appl. Environ. Microbiol. 66:5053–5065. https://doi.org/10.1128/AEM.66.11.5053-5065.2000
Ghylin TW, Garcia SL, Moya F et al (2014) Comparative single-cell genomics reveals potential ecological niches for the freshwater acI Actinobacteria lineage. ISME J 8:2503–2516. https://doi.org/10.1038/ismej.2014.135
Garcia SL, McMahon KD, Martinez-Garcia M et al (2013) Metabolic potential of a single cell belonging to one of the most abundant lineages in freshwater bacterioplankton. ISME J 7:137–147. https://doi.org/10.1038/ismej.2012.86
Zeng D-N, Fan Z-Y, Chi L et al (2013) Analysis of the bacterial communities associated with different drinking water treatment processes. World J. Microbiol. Biotechnol. 29:1573–1584. https://doi.org/10.1007/s11274-013-1321-5
Hahn MW, Lünsdorf H, Wu Q et al (2003) Isolation of novel ultramicrobacteria classified as Actinobacteria from five freshwater habitats in Europe and Asia. Appl. Environ. Microbiol. 69:1442–1451. https://doi.org/10.1128/AEM.69.3.1442-1451.2003
Okazaki Y, Fujinaga S, Tanaka A et al (2017) Ubiquity and quantitative significance of bacterioplankton lineages inhabiting the oxygenated hypolimnion of deep freshwater lakes. ISME J. https://doi.org/10.1038/ismej.2017.89
Clum A, Tindall BJ, Sikorski J et al (2009) Complete genome sequence of Pirellula staleyi type strain (ATCC 27377). Stand. Genomic Sci. 1:308–316. https://doi.org/10.4056/sigs.51657
Wilmotte A, Laughinghouse HDI, Capelli C et al (2017) Taxonomic identification of cyanobacteria by a polyphasic approach. In: Kurmayer R, Sivonen K, Wilmotte A, Salmaso N (eds) Molecular tools for the detection and quantification of toxigenic cyanobacteria. John Wiley, Hoboken, pp 79–119
Plummer E, Twin J, Bulach DM et al (2015) A comparison of three bioinformatics pipelines for the analysis of preterm gut microbiota using 16S rRNA gene sequencing data. J Proteomics Bioinformatics. https://doi.org/10.4172/jpb.1000381
Xiao X, Sogge H, Lagesen K et al (2014) Use of high throughput sequencing and light microscopy show contrasting results in a study of phytoplankton occurrence in a freshwater environment. PLoS One 9:e106510. https://doi.org/10.1371/journal.pone.0106510
Kleinteich J, Hildebrand F, Wood SA et al (2014) Diversity of toxin and non-toxin containing cyanobacterial mats of meltwater ponds on the Antarctic Peninsula: a pyrosequencing approach. Antarct. Sci. 26:521–532. https://doi.org/10.1017/S0954102014000145
Jasser I, Callieri C (2016) Picocyanobacteria—the smallest cell-size cyanobacteria. In: Meriluoto J, Spoof L, Codd GA (eds) Handbook on cyanobacterial monitoring and cyanotoxin analysis1st edn. Wiley, Chichester, pp 19–27
Sivonen K, Carmichael WW, Namikoshi M et al (1990) Isolation and characterization of hepatotoxic microcystin homologs from the filamentous freshwater cyanobacterium Nostoc sp. strain 152. Appl Environ Microbiol 56:2650–2657
Bernard C, Ballot A, Thomazeau S et al (2017) Appendix 2. Cyanobacteria associated with the production of cyanotoxins. In: Meriluoto J, Spoof L, Codd GA (eds) Handbook on cyanobacterial monitoring and cyanotoxin analysis. Wiley, Hoboken, pp 501–525
D’Alelio D, Salmaso N, Gandolfi A (2013) Frequent recombination shapes the epidemic population structure of Planktothrix (Cyanoprokaryota) in Italian subalpine lakes. J. Phycol. 49:1107–1117. https://doi.org/10.1111/jpy.12116
Shih PM, Hemp J, Ward LM et al (2017) Crown group Oxyphotobacteria postdate the rise of oxygen. Geobiology 15:19–29. https://doi.org/10.1111/gbi.12200
Di Rienzi SC, Sharon I, Wrighton KC et al (2013) The human gut and groundwater harbor non-photosynthetic bacteria belonging to a new candidate phylum sibling to Cyanobacteria. eLife 2:e01102. https://doi.org/10.7554/eLife.01102
Monchamp M-E, Walser J-C, Pomati F, Spaak P (2016) Sedimentary DNA reveals cyanobacterial community diversity over 200 years in two perialpine lakes. Appl. Environ. Microbiol. 82:6472–6482. https://doi.org/10.1128/AEM.02174-16
Acknowledgements
Investigations were carried out in the framework of the LTER (Long Term Ecological Research) Italian network, site Southern Alpine lakes, IT08-000-A (http://www.lteritalia.it/), with the support of the ARPA Veneto (Giorgio Franzini and colleagues). We thank our colleagues in FEM, in particular Lorena Ress, Milva Tarter and Andrea Zampedri, for their support in the field and/or laboratory activities. We are grateful to Veronica De Sanctis and Roberto Bertorelli (NGS Facility at the Centre for Integrative Biology and LaBSSAH, University of Trento) for HTS analyses and helpful discussions. The activity was supported by a PhD fellowship (FIRS>T) to C.C. from the E. Mach Foundation – Istituto Agrario di S. Michele all’Adige. We thank the European Cooperation in Science and Technology COST Action ES1105 CYANOCOST for networking and knowledge transfer support. We are grateful to three anonymous reviewers for valuable comments and suggestions on an earlier version of the manuscript.
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Salmaso, N., Albanese, D., Capelli, C. et al. Diversity and Cyclical Seasonal Transitions in the Bacterial Community in a Large and Deep Perialpine Lake. Microb Ecol 76, 125–143 (2018). https://doi.org/10.1007/s00248-017-1120-x
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DOI: https://doi.org/10.1007/s00248-017-1120-x