Abstract
The Carpathian Basin is a lowland plain located mainly in Hungary. Due to the nature of the bedrock, alluvial deposits, and a bowl shape, many lakes and ponds of the area are characterized by high alkalinity. In this study, we characterized temporal changes in eukaryal and bacterial community dynamics with high throughput sequencing and relate the changes to environmental conditions in Lake Velence located in Fejér county, Hungary. The sampled Lake Velence microbial populations (algal and bacterial) were analyzed to identify potential correlations with other community members and environmental parameters at six timepoints over 6 weeks in the Spring of 2012. Correlations between community members suggest a positive relationship between certain algal and bacterial populations (e.g. Chlamydomondaceae with Actinobacteria and Acidobacteria), while other correlations allude to changes in these relationships over time. During the study, high nitrogen availability may have favored non-nitrogen fixing cyanobacteria, such as the toxin-producing Microcystis aeruginosa, and the eutrophic effect may have been exacerbated by high phosphorus availability as well as the high calcium and magnesium content of the Carpathian Basin bedrock, potentially fostering exopolymer production and cell aggregation. Cyanobacterial bloom formation could have a negative environmental impact on other community members and potentially affect overall water quality as well as recreational activities. To our knowledge, this is the first prediction for relationships between photoautotrophic eukaryotes and bacteria from an alkaline, Hungarian lake.
Similar content being viewed by others
References
Ács É, Buczkó K, Lakatos G (1994) Changes in the mosaic-like water surfaces of the Lake Velence as reflected by reed periphyton studies. Stud Bot Hung 25:5–19
Ács É, Borsodi AK, Makk J, Molnár P, Mózes A, Rusznyák A et al (2003) Algological and bacteriological investigations on reed periphyton in Lake Velencei, Hungary. Hydrobiologia 506:549–557
Amaral-Zettler LA, Zettler ER, Theroux SM, Palacios C, Aguilera A, Amils R (2010) Microbial community structure across the tree of life in the extreme Río Tinto. ISME J 5:42–50
Amin SA, Parker MS, Armbrust EV (2012) Interactions between diatoms and bacteria. Microbiol Mol Biol Rev 76:667–684
Baker GC, Smith JJ, Cowan DA (2003) Review and re-analysis of domain-specific 16S primers. J Microbiol Methods 55:541–555
Baldi A, Kisbenedek T (2000) Bird species numbers in an archipelago of reeds at Lake Velence, Hungary. Glob Ecol Biogeogr 9:451–461
Barnhart EP, De León KB, Ramsay BD, Cunningham AB, Fields MW (2013) Investigation of coal-associated bacterial and archaeal populations from a diffusive microbial sampler (DMS). Int J Coal Geol 115:64–70
Bell WH (1983) Bacterial utilization of algal extracellular products. III: the specificity of algal-bacterial interaction. Limnol Oceanogr 28:1131–1143
Bell TAS, Prithiviraj B, Wahlen BD, Fields MW, Peyton BM (2016) A lipid-accumulating alga maintains growth in outdoor, alkaliphilic raceway pond with mixed microbial communities. Front Microbiol 6:497
Berry D, Widder S (2014) Deciphering microbial interactions and detecting keystone species with co-occurrence networks. Front Microbiol 5:219
Bertilsson S, Jones BJ (2003) Supply of dissolved organic matter to aquatic ecosystems. In: Findlay SEG, Sinsabaugh RL (eds) Aquatic ecosystems. Academic Press, New York, pp 3–24
Borics G, Tóthmérész B, Lukács BA, Várbíró G (2012) Functional groups of phytoplankton shaping diversity of shallow lake ecosystems. Hydrobiologia 698:251–262
Borics G, Acs E, Boros E, Er T, Grigorszky I, Kiss KT et al (2016) Water bodies in Hungary—an overview of their management and present state. Hung J Hydrol 96:57–67
Boromisza Z, Torok EP, Acs T (2014) Lakeshore-restoration: landscape ecology-land use: assessment of shore-sections, being suitable for restoration, by the example of Lake Velence (Hungary). Carpathian J Earth Environ Sci 9:179–188
Boros E, Nagy T, Pigniczki C, Kotymán L (2008) The effect of aquatic birds on the nutrient load and water quality of soda pans in Hungary. Acta Zool Acad Sci Hung 54:207–224
Boros E, Horváth Z, Wolfram G, Vörös L (2014) Salinity and ionic composition of the shallow astatic soda pans in the Carpathian Basin. Ann Limnol—Int J Limnol 50:59–69
Borsodi AK, Micsinai A, Rusznyák A, Vladár P, Kovács G, Tóth EM et al (2005) Diversity of alkaliphilic and alkalitolerant bacteria cultivated from decomposing reed rhizomes in a Hungarian soda lake. Microb Ecol 50:9–18
Bowen De León K, Ramsay BD, Fields MW (2012) Quality-score refinement of SSU rRNA gene pyrosequencing differs across gene region for environmental samples. Microb Ecol 64:499–508
Brussaard CPD (2004) Viral control of phytoplankton populations: a review. J Eukaryot Microbiol 51:125–138
Camacho A, Vicente E, Miracle MR (2001) Ecology of Cryptomonas at the chemocline of a karstic sulfate-rich lake. Mar Freshw Res 52:805–815
Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2010a) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26:266–267
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al (2010b) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336
Davis TW, Berry DL, Boyer GL, Gobler CJ (2009) The effects of temperature and nutrients on the growth and dynamics of toxic and non-toxic strains of Microcystis during cyanobacteria blooms. Harmful Algae 8:715–725
De Jesús-Laboy KM, Godoy-Vitorino F, Piceno YM, Tom LM, Pantoja-Feliciano IG, Rivera-Rivera MJ et al (2012) Comparison of the fecal microbiota in feral and domestic goats. Genes 3:1–18
De Senerpont Domis LN, Elser JJ, Gsell AS, Huszar VLM, Ibelings BW, Jeppesen E et al (2012) Plankton dynamics under different climatic conditions in space and time. Freshw Biol 58:463–482
Dodds WK, Robinson CT, Gaiser EE, Hansen GJ, Powell H, Smith JM et al (2012) Surprises and insights from long-term aquatic data sets and experiments. Bioscience 62:709–721
Eaton AD, Franson MAH (2005) Standard methods for the examination of water & wastewater. Ignatius Press, San Francisco
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461
Farkas O, Gyémant G, Hajdú G, Gonda S, Parizsa P, Horgos T et al (2014) Variability of microcystins and its synthetase gene cluster in Microcystis and Planktothrix water blooms in shallow lakes of Hungary. Acta Biol Hung 65:227–239
Felföldi T, Somogyi B, Márialigeti K, Vörös L (2009) Characterization of photoautotrophic picoplankton assemblages in turbid, alkaline lakes of the Carpathian Basin (Central Europe). J Limnol 68:385–395
Fields MW, Yan T, Rhee S-K, Carroll SL, Jardine PM, Watson DB et al (2005) Impacts on microbial communities and cultivable isolates from groundwater contaminated with high levels of nitric acid-uranium waste. FEMS Microbiol Ecol 53:417–428
Fields MW, Bagwell CE, Carroll SL, Yan T, Liu X, Watson DB et al (2006) Phylogenetic and functional biomakers as indicators of bacterial community responses to mixed-waste contamination. Environ Sci Technol 40:2601–2607
Flynn KJ (1998) Estimation of kinetic parameters for the transport of nitrate and ammonium into marine phytoplankton. Mar Ecol Prog Ser 169:13–28
Foster RA, Kuypers MMM, Vagner T, Paerl RW, Musat N, Zehr JP (2011) Nitrogen fixation and transfer in open ocean diatom–cyanobacterial symbioses. ISME J 5:1484–1493
Friedman J, Alm EJ (2012) Inferring correlation networks from genomic survey data. PLoS Comput Biol 8:e1002687
Fritsche TR, Horn M, Seyedirashti S, Gautom RK, Schleifer KH, Wagner M (1999) In situ detection of novel bacterial endosymbionts of Acanthamoeba spp. phylogenetically related to members of the order Rickettsiales. Appl Environ Microbiol 65:206–212
Gobler CJ, Burkholder JM, Davis TW, Harke MJ, Johengen T, Stow CA et al (2016) The dual role of nitrogen supply in controlling the growth and toxicity of cyanobacterial blooms. Harmful Algae 54:87–97
Goecke F, Thiel V, Wiese J, Labes A, Imhoff JF (2013) Algae as an important environment for bacteria-phylogenetic relationships among new bacterial species isolated from algae. Phycologia 52:14–24
Grant WD (2006) Alkaline environments and biodiversity. In: Gerday C, Glansdorff N (eds) Extremophiles. EOLSS, Developed under UNESCO. Eolss Publishers, Oxford, UK
Green DH, Echavarri-Bravo V, Brennan D, Hart MC (2015) Bacterial diversity associated with the Coccolithophorid Algae Emiliania huxleyi and Coccolithus pelagicus f. braarudii. Science 2015:194540
Grossart HP, Simon M (2007) Interactions of planktonic algae and bacteria: effects on algal growth and organic matter dynamics. Aquat Microb Ecol 47:163–176
Gupta N, Pant SC, Vijayaraghavan R, Rao PVL (2003) Comparative toxicity evaluation of cyanobacterial cyclic peptide toxin microcystin variants (LR, RR, YR) in mice. Toxicology 188:285–296
Haas J (2012) Geology of Hungary. Springer, Berlin
Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G et al (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 21:494–504
Habermehl GG, Krebs HC, Nemes P (1997) Occurrence of toxin producing cyanobacteria in Hungary. Isolation, separation and identification of microcystins. Verl Z Naturforschung 52:107–109
Hall RI, Smol JP (1992) A weighted-averaging regression and calibration model for inferring total phosphorus concentration from diatoms in British Columbia (Canada) lakes. Freshw Biol 27:417–434
Hamilton DP, Salmaso N, Paerl HW (2016) Mitigating harmful cyanobacterial blooms: strategies for control of nitrogen and phosphorus loads. Aquat Ecol 50:351–366
Harke MJ, Steffen MM, Gobler CJ, Otten TG, Wilhelm SW, Wood SA et al (2016) A review of the global ecology, genomics, and biogeography of the toxic cyanobacterium, Microcystis spp. Harmful Algae 54:4–20
Hem JD (1985) Study and interpretation of the chemical characteristics of natural water. Department of the Interior, U.S. Geological Survey, Alexandria
Hill MO (1973) Diversity and evenness: a unifying notation and its consequences. Ecology 54:427–432
Hill RW, White BA, Cottrell MT, Dacey JW (1998) Virus-mediated total release of dimethylsulfoniopropionate from marine phytoplankton: a potential climate process. Aquat Microb Ecol 14:1–6
Hindák F, Hindáková A (2008) Morphology and taxonomy of some rare chlorococcalean algae (Chlorophyta). Biologia 63:781–790
Horváth I, Daridáne M, Dudko A, Gyalog L, Ódor L (2004) A Velencei-tólimnogeológiája. In: Gyalog L, Horváth I (eds) A Velencei-hegység és a Balatonfő földtana. Geological Institute of Hungary, Budapest
Hudson JJ, Taylor WD, Schindler DW (2000) Phosphate concentrations in lakes. Nature 406:54–56
Imhoff JF, Sahl HG, Soliman G (1979) The Wadi Natrun: chemical composition and microbial mass developments in alkaline brines of eutrophic desert lakes. Geomicrobiol J 1:219–234
Jiang Y, Ji B, Wong RNS, Wong MH (2008) Statistical study on the effects of environmental factors on the growth and microcystins production of bloom-forming cyanobacterium—Microcystis aeruginosa. Harmful Algae 7:127–136
Jost L (2006) Entropy and diversity. Oikos 113:363–375
Juggins S (2012) Rioja: analysis of quaternary science data version: 0.7–3
Kalakoutskii LV, Zenova GM, Soina VS (1990) Associations of actinomycetes with algae. Actinomycetes 1:27–42
Kós P, Gorzó G, Surányi G, Borbély G (1995) Simple and efficient method for isolation and measurement of cyanobacterial hepatotoxins by plant tests (Sinapis alba L.). Anal Biochem 225:49–53
Larsen JB, Larsen A, Bratbak G, Sandaa RA (2008) Phylogenetic analysis of members of the Phycodnaviridae virus family, using amplified fragments of the major capsid protein gene. Appl Environ Microbiol 74:3048–3057
Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120
López-Archilla AI, Moreira D, López-García P, Guerrero C (2004) Phytoplankton diversity and cyanobacterial dominance in a hypereutrophic shallow lake with biologically produced alkaline pH. Extremophiles 8:109–115
Lozupone C, Knight R (2005) Unifrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235
Martínez JM, Schroeder DC, Larsen A et al (2007) Molecular dynamics of Emiliania huxleyi and cooccurring viruses during two separate mesocosm studies. Appl Environ Microbiol 73:554–562
Mieczan T (2008) Chara and Ceratophyllum as a substrate for ciliates in two shallow lakes (Łęczna-Włodawa Lakeland, eastern Poland). Int J Oceanogr Hydrobiol 37:1–9
Newton RJ, Jones SE, Eiler A, McMahon KD, Bertilsson S (2011) A guide to the natural history of freshwater lake bacteria. Microbiol Mol Biol Rev 75:14–49
Odum EP, Finn JT, Franz EH (1979) Perturbation theory and the subsidy-stress gradient. Bioscience 29:349–352
Oksanen J (2011) Multivariate analysis of ecological communities in R: vegan tutorial. R package version, 2.0–1
Paerl HW, Otten TG (2013) Harmful cyanobacterial blooms: causes, consequences, and controls. Microb Ecol 65:995–1010
Paerl HW, Paul VJ (2012) Climate change: links to global expansion of harmful cyanobacteria. Water Res 46:1349–1363
Paerl HW, Fulton RS, Moisander PH, Dyble J (2001) Harmful freshwater algal blooms, with an emphasis on cyanobacteria. Sci World J 1:76–113
Paerl HW, Xu H, McCarthy MJ, Zhu G, Qin B, Li Y et al (2011) Controlling harmful cyanobacterial blooms ina hyper-eutrophic lake (Lake Taihu, China): the need for a dual nutrient (N & P) management strategy. Water Res 45:1973–1983
Paerl HW, Xu H, Hall NS, Zhu G, Qin B, Wu Y et al (2014) Controlling cyanobacterial blooms in hypertrophic Lake Taihu, China: will nitrogen reductions cause replacement of non-N-2 fixing by N-2 fixing taxa? PLoS ONE 9:e113123
Pálffy K, Felföldi T, Mentes A, Horváth H, Márialigeti K, Boros E et al (2014) Unique picoeukaryotic algal community under multiple environmental stress conditions in a shallow, alkaline pan. Extremophiles 18:111–119
Ramanan R, Kang Z, Kim B-H, Cho D-H, Jin L, Oh H-M et al (2015) Phycosphere bacterial diversity in green algae reveals an apparent similarity across habitats. Algal Res 8:140–144
Reskóné MN, Torokne AK (2000) Toxic Microcystis aeruginosa in Lake Velencei. Environ Toxicol 15:554–557
Reti KL, Thomas MC, Yanke LJ, Selinger LB, Inglis GD (2013) Effect of antimicrobial growth promoter administration on the intestinal microbiota of beef cattle. Gut Pathog 5:8
Rhodes CJ, Martin AP (2010) The influence of viral infection on a plankton ecosystem undergoing nutrient enrichment. J Theor Biol 265:225–237
Ritchie RJ, Trautman DA, Larkum A (2001) Phosphate limited cultures of the cyanobacterium Synechococcus are capable of very rapid, opportunistic uptake of phosphate. New Phytol 152:189–201
Robarts RD, Zohary T (1987) Temperature effects on photosynthetic capacity, respiration, and growth rates of bloom-forming cyanobacteria. N Z J Mar Freshwat Res 21:391–399
Runnegar M, Berndt N, Kaplowitz N (1995) Microcystin uptake and inhibition of protein phosphatases: effects of chemoprotectants and self-inhibition in relation to known hepatic transporters. Toxicol Appl Pharmacol 134:264–272
Sapp M, Schwaderer AS, Wiltshire KH, Hoppe H-G, Gerdts G, Wichels A (2007) Species-specific bacterial communities in the phycosphere of microalgae? Microb Ecol 53:683–699
Seyedsayamdost MR, Case RJ, Kolter R, Clardy J (2011) The Jekyll-and-Hyde chemistry of Phaeobacter gallaeciensis. Nat Chem 3:331–335
Shen H, Song L (2007) Comparative studies on physiological responses to phosphorus in two phenotypes of bloom-forming Microcystis. Hydrobiologia 592:475–486
Shepherd ML, Swecker WS Jr, Jensen RV, Ponder MA (2011) Characterization of the fecal bacteria communities of forage-fed horses by pyrosequencing of 16S rRNA V4 gene amplicons. FEMS Microbiol Lett 326:62–68
Short SM (2012) The ecology of viruses that infect eukaryotic algae. Environ Microbiol 14:2253–2271
Stearns JC, Lynch MDJ, Senadheera DB, Tenenbaum HC, Goldberg MB, Cvitkovitch DG et al (2011) Bacterial biogeography of the human digestive tract. Sci Rep 1:1–9
Strayer DL, Dudgeon D (2010) Freshwater biodiversity conservation: recent progress and future challenges. J N Am Benthol Soc 29:344–358
Szabó A, Korponai K, Kerepesi C, Somogyi B, Vörös L, Bartha D et al (2017) Soda pans of the Pannonian steppe harbor unique bacterial communities adapted to multiple extreme conditions. Extremophiles 21:639–649
Tarakhovskaya ER, Maslov YI, Shishova MF (2007) Phytohormones in algae. Russ J Plant Physiol 54:163–170
Van Etten JL, Lane LC, Meints RH (1991) Viruses and viruslike particles of eukaryotic algae. Microbiol Rev 55:586–620
Vasas G, Szydlowska D, Gáspár A, Welker M, Trojanowicz M, Borbély G (2006) Determination of microcystins in environmental samples using capillary electrophoresis. J Biochem Biophys Methods 66:87–97
Vasas G, Bácsi I, Surányi G, Hamvas MM, Máthé C, Nagy SA et al (2010) Isolation of viable cell mass from frozen Microcystis viridis bloom containing microcystin-RR. Hydrobiologia 639:147–151
Vasas G, Farkas O, Borics G, Felföldi T, Sramkó G, Batta G et al (2013) Appearance of Planktothrix rubescens bloom with [D-Asp3, Mdha7]MC–RR in gravel pit pond of a shallow lake-dominated area. Toxins 5:2434–2455
Vörös L, Gulyás P, Németh J (2006) Occurrence, dynamics and production of picoplankton in Hungarian shallow lakes. Int Rev Gesamten Hydrobiol Hydrogr 76:617–629
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267
Water Management Directorate of VITUKI Environmental Protection and Water Management Research Institute on behalf of the Ministry for Environment and Water (2006) Groundwaters in Hungary II. In: H.M.F. Environment Water (eds)
Weitz J, Wilhelm S (2012) Ocean viruses and their effects on microbial communities and biogeochemical cycles. F1000 Biol Rep 4:1–8
Wetzel RG (2001) Limnology, 3rd edn. Academic Press, London
Wilhelm SW, Suttle CA (1999) Viruses and nutrient cycles in the sea: viruses play critical roles in the structure and function of aquatic food webs. Bioscience 49:781–788
Wommack KE, Colwell RR (2000) Virioplankton: viruses in aquatic ecosystems. Microbiol Mol Biol Rev 64:69–114
Wood SA, Borges H, Puddick J, Biessy L, Atalah J, Hawes I et al (2016) Contrasting cyanobacterial communities and microcystin concentrations in summers with extreme weather events: insights into potential effects of climate change. Hydrobiologia 785:71–89
Záray G, Kröpfl K, Szabó K, Taba G, Acs E, Berlinger B et al (2005) Comparison of freshwater biofilms grown on polycarbonate substrata in Lake Velence (Hungary) and Lake Mogan (Turkey). Microchem J 79:145–148
Zhao L, Lu L, Li M, Xu Z, Zhu W (2011) Effects of Ca and Mg levels on colony formation and EPS content of cultured M. aeruginosa. Procedia Environ Sci 10:1452–1458
Zhou J, Bruns MA, Tiedje JM (1996) DNA recovery from soils of diverse composition. Appl Environ Microbiol 62:316–322
Acknowledgements
The authors wish to thank Katalin Barkács and Laura Jurecska (Cooperative Research Centre for Environmental Sciences, Budapest, Hungary) for the chemical analysis of water samples. We would also like to thank Frank W. Schneider Agriculture Specialist, for U.S. Customs and Border Protection for his assistance and Dr. Bharath Prithiviraj with the Plant Biology Division at the Samuel Roberts Noble Foundation Inc. for his bioinformatics expertise. Thanks are also due to Devon Andor Bell, Susi Szeremy, Ajna Akantisz, Hugh MacMurray, and Shane Mortensen for sampling assistance.
Funding
Support was provided by the US Department of Energy-Advancements in Sustainable Algal Production (ASAP) program under contract DE-EE0005993. T.S.A. Bell was also partially supported by the NSF IGERT Program in Geobiological Systems (DGE 0654336). T. Felföldi was supported by the János Bolyai Research Scholarship of the Hungarian Academy of Sciences. Additional support was provided by the National Research, Development, and Innovation Office of Hungary (Grant Number K 116275). G. Vasas was supported by the National Research, Development, and Innovation Office of Hungary (NKFIH-119647).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Bell, T.A.S., Sen-Kilic, E., Felföldi, T. et al. Microbial community changes during a toxic cyanobacterial bloom in an alkaline Hungarian lake. Antonie van Leeuwenhoek 111, 2425–2440 (2018). https://doi.org/10.1007/s10482-018-1132-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10482-018-1132-7