Abstract
In Lake Biwa, picocyanobacteria blooms usually occur during the summer–autumn thermal stratification period. Intriguingly, a novel bloom was detected in winter 2015–2016, in which picocyanobacterial cell density increased by one order of magnitude despite lower water temperature, suggesting the possibility that “cold-water-preference” species dominate in the picocyanobacterial community. In the present study, we investigated the phylogenetic diversity of picocyanobacteria in Lake Biwa by analyzing the 16S rRNA gene. We found that the picocyanobacterial community were highly diverse in Lake Biwa, with eight Synechococcus-related operational taxonomic units (OTUs) detected in different seasons. These OTUs fell into distinct phylogenetic groups, and the majority were closely related to clusters reported previously. Notably, OTU04, detected during the winter bloom, was highly affiliated with sequences found in a variety of lakes, such as Tibetan lakes and Lake Superior, where the water bodies generally have a low trophic state and temperature, and different concentrations of total dissolved solids. Thus, we inferred that the group containing OTU04 may be a psychrotolerant lineage that is widely distributed in oligotrophic water systems with low–intermediate salinity.
References
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res 25:3389–3402
Beardall J, Raven JA (2004) Potential effects of global change on microalgal photosynthesis, growth and ecology. Phycologia 43:26–40
Brunskill GJ, Ludlam SD (1969) Fayetteville Green Lake, New York. I Physical and chemical limnology. Limnol Oceanogr 14:817–829
Cai Y, Kong F (2013) Diversity and dynamics of picocyanobacteria and the bloom-forming cyanobacteria in a large shallow eutrophic lake (Lake Chaohu, China). J Limnol 72:473–484
Callieri C (2008) Picophytoplankton in freshwater ecosystems: the importance of small-sized phototrophs. Freshw Rev 1:1–28
Callieri C, Coci M, Corno G, Modenutti B, Balseiro E, Bertoni R (2013) Phylogenetic diversity of nonmarine picocyanobacteria. FEMS Microbiol Ecol 85:293–301
Chapra SC, Dove A, Warren GJ (2012) Long-term trends of Great Lakes major ion chemistry. J Great Lakes Res 38:550–560
Choi DH, Noh JH, Shim J (2013) Seasonal changes in picocyanobacterial diversity as revealed by pyrosequencing in temperate waters of the East China Sea and the East Sea. Aquat Microb Ecol 71:75–90
Cottrell MT, Kirchman DL (2009) Photoheterotrophic microbes in the Arctic Ocean in summer and winter. Appl Environ Microbiol 75:4958–4966
Crosbie ND, Pöckl M, Weisse T (2003) Dispersal and phylogenetic diversity of nonmarine picocyanobacteria, inferred from 16S rRNA gene and cpcBA intergenic spacer sequence analyses. Appl Environ Microb 69:5716–5721
Dove A, Chapra SC (2015) Long-term trends of nutrients and trophic response variables for the Great Lakes. Limnol Oceanogr 60:696–721
Dupont F, Chittibabu P, Fortin V, Rao YR, Lu Y (2012) Assessment of a NEMO-based hydrodynamic modelling system for the Great Lakes. Water Qual Res J Can 47(3–4):198–214
Edgar RC (2018) Updating the 97% identity threshold for 16S ribosomal RNA OTUs. Bioinformatics 34(14):2371–2375
Ernst A, Becker S, Wollenzien UI, Postius C (2003) Ecosystem-dependent adaptive radiations of picocyanobacteria inferred from 16S rRNA and ITS-1 sequence analysis. Microbiology 149:217–228
Guildford S, Hecky RE (2000) Total nitrogen, total phosphorus, and nutrient limitation in lakes and oceans: Is there a common relationship? Limnol Oceanogr 45:1213–1223
Huang S, Liu Y, Hu A, Liu X, Chen F, Yao T, Jiao N (2014) Genetic diversity of picocyanobacteria in Tibetan lakes: assessing the endemic and universal distributions. Appl Environ Microbiol 80:7640–7650
Ivanikova NV, Popels LC, McKay RM, Bullerjahn GS (2007) Lake Superior supports novel clusters of cyanobacterial picoplankton. Appl Environ Microbiol 73:4055–4065
Ji C, Hodoki Y, Ushio M, Nakano S (2020) Influence of potential grazers on picocyanobacterial abundance in Lake Biwa revealed with empirical dynamic modeling. Inland Waters. https://doi.org/10.1080/20442041.2020.1711682
Jodłowska S, Śliwińska S (2014) Effects of light intensity and temperature on the photosynthetic irradiance response curves and chlorophyll fluorescence in three picocyanobacterial strains of Synechococcus. Photosynthetica 52:223–232
Kojima H, Tokizawa R, Kogure K, Kobayashi Y, Itoh M, Shiah FK, Okuda N, Fukui M (2014) Community structure of planktonic methane-oxidizing bacteria in a subtropical reservoir characterized by dominance of phylotype closely related to nitrite reducer. Sci Rep 4:5728
Komárek J, Kaštovský J, Jezberová J (2011) Phylogenetic and taxonomic delimitation of the cyanobacterial genera Aphanothece and Anathece. Eur J Phycol 46:315–326
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 35:1547–1549
Lovejoy C, Vincent WF, Bonilla S, Roy S, Martineau MJ, Terrado R, Potvin M, Massana R, Pedrós-Alió C (2007) Distribution, phylogeny, and growth of cold-adapted picoprasinophytes in Arctic seas. J Phycol 43:78–89
Maeda H, Kawai A, Tilzer MM (1992) The water bloom of cyanobacterial picoplankton in Lake Biwa, Japan. Hydrobiologia 248:93–103
Meyer KM, Macalady JL, Fulton JM, Kump LR, Schaperdoth I, Freeman KH (2011) Carotenoid biomarkers as an imperfect reflection of the anoxygenic phototrophic community in meromictic Fayetteville Green Lake. Geobiology 9:321–329
Nagata T (1986) The seasonal abundance and vertical distribution of the <3-µm phytoplankton in the north basin of Lake Biwa. Ecol Res 1:207–221
Nakano S, Tanaka K, Sono T, Wakabayashi T, Ichise S, Yamanaka S, Kaneda E, Yada M, Naitoh M, Kawabe K, Maehata K, Fujiwara N, Maeda N, Nomura K, Nakanishi M (1996) Seasonal Changes in Horizontal Distribution of Algal Picoplankton in Lake Biwa with Special Reference to Water Temperature, Nutrient Levels and Heterotrophic Flagellates. Jpn J Limnol 57:49–55
Nübel U, Garcia-Pichel F, Muyzer G (1997) PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl Environ Microbiol 63:3327–3332
Ohki K, Yamada K, Kamiya M, Yoshikawa S (2012) Morphological, phylogenetic and physiological studies of pico-cyanobacteria isolated from the halocline of a saline meromictic lake, Lake Suigetsu, Japan. Microbes Environ 27:171–178
Price MN, Dehal PS, Arkin AP (2010) FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS ONE 5(3):e9490
R Development Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Rajaniemi-Wacklin P, Rantala A, Kuuppo P, Haukka K, Sivonen K (2008) Cyanobacterial community composition in shallow, eutrophic Lake Tuusulanjärvi studied by microscopy, strain isolation, DGGE and cloning. Algol Stud 126:137–157
Robertson BR, Tezuka N, Watanabe MM (2001) Phylogenetic analyses of Synechococcus strains (cyanobacteria) using sequences of the 16S rDNA and part of the phycocyanin operon reveal multiple evolutionary lines and reflect phycobilin content. Int J Syst Evol Micr 51:861–871
Rognes T, Flouri T, Nichols B, Quince C, Mahé F (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ 4:e2584
Śliwińska-Wilczewska S, Maculewicz J, Felpeto B, Aldo & Latała, Adam, (2018) Allelopathic and Bloom-Forming Picocyanobacteria in a Changing World. Toxins 10(1):48
Stockner JG (1988) Phototrophic picoplankton: an overview from marine and freshwater ecosystems. Limnol Oceanogr 33:765–775
Stockner JG (1991) Autotrophic picoplankton in freshwater ecosystems: the view from the summit. Int Rev ges Hydrobiol 76:483–492
Stockner JG, Antia NJ (1986) Algal picoplankton from marine and freshwater systems: a multidisciplinary perspective. Can J Aquat Sci 43:2472–2503
Stockner J, Callieri C, Cronberg G (2000) Picoplankton and other non-bloom-forming cyanobacteria in lakes. In: Whitton BA, Potts M (eds) The Ecology of Cyanobacteria. Kluwer Academic Publishers, Dordrecht, pp 195–231
Vörös L, Mózes A, Somogyi B (2009) A five-year study of autotrophic winter picoplankton in Lake Balaton, Hungary. Aquat Ecol 43:727–734
Wakabayashi T, Ichise S (2004) Seasonal variation of phototrophic picoplankton in Lake Biwa (1994–1998). Hydrobiologia 528:1–16
Weisse T (1993) Dynamics of autotrophic picoplankton in marine and freshwater ecosystems. Adv Microb Ecol 13:327–370
Wu QL, Xing P, Liu WT (2010) East Tibetan lakes harbour novel clusters of picocyanobacteria as inferred from the 16S–23S rRNA internal transcribed spacer sequences. Microb Ecol 59:614–622
Xing P, Hahn MW, Wu QL (2009) Low taxon richness of bacterioplankton in high-altitude lakes of the eastern Tibetan Plateau, with a predominance of Bacteroidetes and Synechococcus spp. Appl Environ Microbiol 75:7017–7025
Xu Y, Jiao N, Chen F (2015) Novel psychrotolerant picocyanobacteria isolated from Chesapeake Bay in the winter. J Phycol 51:782–790
Yu G, Smith DK, Zhu H, Guan Y, Lam TTY (2017) ggtree: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol Evol 8:28–36
Acknowledgments
We are grateful to Drs. Yukiko Goda and Tetsushi Akatsuka and the crew of our sampling vessel “HASU” for providing technical assistance during sample collection. We also thank Dr. Yusuke Okazaki, Dr. Indranil Mukherjee, and Mr. Fujinaga Shohei for their valuable help during sampling. This work was partly supported by KAKENHI, Grants-in-Aid for Scientific Research, grant numbers 17K19289 and 19H03302 from the Japan Society for the Promotion of Science, and the Environment Research and Technology Development Fund No. 5-1607 of the Ministry of the Environment.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Handling Editor: Kunihiro OKANO.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Cai, J., Hodoki, Y. & Nakano, Si. Phylogenetic diversity of the picocyanobacterial community from a novel winter bloom in Lake Biwa. Limnology 22, 161–167 (2021). https://doi.org/10.1007/s10201-020-00649-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10201-020-00649-5