981
Views
15
CrossRef citations to date
0
Altmetric
Original Articles

Contrasting histories of microcystin-producing cyanobacteria in two temperate lakes as inferred from quantitative sediment DNA analyses

, , , , , , & show all

References

  • Adams KE, Taranu ZE, Zurawell R, Cumming BF, Gregory-Eaves I. 2014. Insights for lake management gained when paleolimnological and water column monitoring studies are combined: a case study from Baptiste Lake. Lake Reserv Manag. 30:11–22.
  • Benoit G, Rozan TF. 2001. 210Pb and 137Cs dating methods in lakes: a retrospective study. J Paleolimnol. 25:455–465.
  • Beversdorf LJ, Chaston SD, Miller TR, McMahon KD, Hrudey S. 2015. Microcystin mcyA and mcyE gene abundances are not appropriate indicators of microcystin concentrations in lakes. PLoS One. 10(5):e0125353.
  • Bird DF, Kalff J. 1984. Empirical relationships between bacterial abundance and chlorophyll concentration in fresh and marine waters. Can J Fish Aquat Sci. 41(7):1015–1023.
  • Brazeau ML, Blais JM, Paterson AM, Keller W, Poulain AJ. 2013. Evidence for microbially mediated production of elemental mercury (Hg0) in subarctic lake sediments. Appl Geochem. 37:142–148.
  • Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, et al. 2009. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem. 55(4):611–622.
  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 7(5):335–336.
  • Chen H, Burke JM, Dinsmore WP, Prepas EE, Fedorak PM. 2007. First assessment of cyanobacterial blooms and microcystin-LR in the Canadian portion of Lake of the Woods. Lake Reserv Manag. 23:169–178.
  • Chorus I, Bartram J. 1999. Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management. World Health Organization, E&FN Spon, Routledge, London, UK.
  • Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y, Brown CT, Porras-Alfaro A, Kuske CR, Tiedje JM. 2014. Ribosomal database project: data and tools for high throughput rRNA analysis. Nucl Acids Res. 42(D1):D633–D642.
  • Coolen M. 2004. Combined DNA and lipid analyses of sediments reveal changes in Holocene haptophyte and diatom populations in an Antarctic lake. Earth Planet Sci Lett. 223(1–2):225–239.
  • Coulon F, Chronopoulou PM, Fahy A, Païssé S, Goñi-Urriza M, Peperzak L, Acuña Alvarez L, McKew BA, Brussaard CPD, Underwood GJC, et al. 2012. Central role of dynamic tidal biofilms dominated by aerobic hydrocarbonoclastic bacteria and diatoms in the biodegradation of hydrocarbons in coastal mudflats. Appl Environ Microbiol. 78(10):3638–3648.
  • DeSellas AM, Paterson AM, Clark BJ, Baratono NG, Sellers TJ. 2009. State of the basin report for Lake of the Woods and Rainy River basin. Multi-Agency Technical Report. http://www.rainylakeconservancy.org/Resources/Documents/2009_State_of_the_Basin_Report.pdf
  • Domaizon I, Savichtcheva O, Debroas D, Arnaud F, Villar C, Pignol C, Alric B, Perga ME. 2013. DNA from lake sediments reveals the long-term dynamics and diversity of Synechococcus assemblages. Biogeosciences. 10(6):3817–3838.
  • Dowd SE, Callaway TR, Wolcott RD, Sun Y, McKeehan T, Hagevoort RG, Edrington TS. 2001. Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). Nucleic Acids Res. 29173–174.
  • Downing JA, Watson SB, McCauley E. 2001. Predicting cyanobacteria dominance in lakes. Can J Fish Aquat Sci. 58(10):1905–1908.
  • Engene N, Gerwick WH. 2011. Intra-genomic 16S rRNA gene heterogeniety in cyanobacterial genomes. Fottea. 11(1):17–24.
  • Fortin N, Aranda-Rodriguez R, Jing H, Pick F, Bird D, Greer CW. 2010. Detection of microcystin-producing cyanobacteria in Missisquoi Bay, Quebec, Canada, using quantitative PCR. Appl Environ Microbiol. 76(15):5105–5112.
  • Funari E, Testai E. 2008. Human health risk assessment related to cyanotoxins exposure. Crit Rev Toxicol. 38(2):97–125.
  • Glew J. 1991. Miniature gravity corer for recovering short sediment cores. J Paleolimnol. 5285–287.
  • Ha JH, Hidaka T, Tsuno H. 2009. Quantification of toxic Microcystis and evaluation of its dominance ratio in blooms using Real-Time PCR. Environ Sci Technol. 43(3):812–818.
  • Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G, Ciulla D, Tabbaa D, Highlander SK, Sodergren E, et al. 2011. Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res. 21(3):494–504.
  • Harke MJ, Steffen MM, Gobler CJ, Otten TG, Wilhelm SW, Wood SA, Paerl HW. 2016. A review of the global ecology, genomics, and biogeography of the toxic cyanobacterium, Microcystis spp. Harmful Algae. 54:4–20.
  • Hickman M, Schweger C, Klarer D. 1990. Baptiste Lake, Alberta: a late holocene history of changes in a lake and its catchment in the southern Boreal forest. J Paleolimnol. 4:253–267.
  • Hisbergues M, Christiansen G, Rouhiainen L, Sivonen K, Börner T. 2003. PCR-based identification of microcystin-producing genotypes of different cyanobacterial genera. Arch Microbiol. 180(6):402–410.
  • Hurt RA, Qiu X, Wu L, Roh Y, Palumbo AV, Tiedje JM, Zhou J. 2001. Simultaneous recovery of RNA and DNA from soils and sediments. Appl Environ Microbiol. 67(10):4495–4503.
  • Hyatt CV, Paterson AM, Rühland KM, Smol JP. 2011. Examining 20th century water quality and ecological changes in the Lake of the Woods, Ontario, Canada: a paleolimnological investigation. J. Great Lakes Res. 37(3):456–469.
  • Jaiswal P, Singh PK, Prasanna R. 2008. Cyanobacterial bioactive molecules: an overview of their toxic properties. Can J Microbiol. 54(9):701–717.
  • Jiang H, Dong H, Yu B, Liu X, Li Y, Ji S, Zhang CL. 2007. Microbial response to salinity change in Lake Chaka, a hypersaline lake on Tibetan plateau. Environ Microbiol. 9(10):2603–2621.
  • Jungblut AD, Hawes I, Mountfort D, Hitzfeld B, Dietrich DR, Burns BP, Neilan BA. 2005. Diversity within cyanobacterial mat communities in variable salinity meltwater ponds of McMurdo Ice Shelf, Antarctica. Environ Microbiol. 7(4):519–529.
  • Kaebernick M, Neilan BA, Borner T, Dittmann E. 2000. Light and the transcriptional response of the microcystin biosynthesis gene cluster. Appl Environ Microbiol. 66(8):3387–3392.
  • Kamenova S, Bartley TJ, Bohan DA, Boutain JR, Colautti RI, Domaizon I, Fontaine C, Lemainque A, Le Viol I, Mollot G, et al. 2017. Invasions toolkit: current methods for tracking the spread and impact of invasive species, Chap 3. In: Advances in ecological research. Cambridge, MA: Academic Press; pp. 85–182. doi:10.1016/bs.aecr.2016.10.009.
  • Kaneko T, Nakajima N, Okamoto S, Suzuki I, Tanabe Y, Tamaoki M, Nakamura Y, Kasai F, Watanabe A, Kawashima K, et al. 2007. Complete genomic structure of the bloom-forming toxic cyanobacterium Microcystis aeruginosa NIES-843. DNA Res. 14(6):247–256.
  • Kleinteich J, Hildebrand F, Wood SA, Ciŕs S, Agha R, Quesada A, Pearce DA, Convey P, K¨Pper FC, Dietrich DR, 2014. Diversity of toxin and non-toxin containing cyanobacterial mats of meltwater ponds on the Antarctic Peninsula: a pyrosequencing approach. Antarct Sci. 26(5):521–532.
  • Koskenniemi K, Lyra C, Rajaniemi-Wacklin P, Jokela J, Sivonen K. 2007. Quantitative real-time PCR detection of toxic Nodularia cyanobacteria in the Baltic Sea. Appl Environ Microbiol. 73(7):2173–2179.
  • Kotak BG, Zurawell RW. 2007. Cyanobacterial toxins in Canadian freshwaters: a review. Lake Reserv Manag. 23(2):109–122.
  • Kyle M, Haande S, Sønstebø J, Rohrlack T. 2015. Amplification of DNA in sediment cores to detect historic Planktothrix occurrence in three Norwegian lakes. J Paleolimnol. 53(1):61–72.
  • Leavitt PR, Hodgson DA. 2002. Sedimentary pigments. In: Tracking environmental change using lake sediments. Dordrecht: Kluwer Academic Publishers.
  • LeBlanc Renaud S, Pick FR, Fortin N. 2011. Effect of light intensity on the relative dominance of toxigenic and nontoxigenic strains of Microcystis aeruginosa. Appl Environ Microbiol. 77(19):7016–7022.
  • Legendre P, Legendre L. 2012. Numerical Ecology. 3rd ed. Amsterdam, The Netherlands: Elsevier.
  • Legrand B, Lamarque A, Sabart M, Latour D. 2017. Benthic archives reveal occurrence and dominance of toxic cyanobacteria in a eutrophic lake over the last 220 years. Toxins. 9(9):271.
  • Lejzerowicz F, Esling P, Majewski W, Szczuciński W, Decelle J, Obadia C, Arbizu PM, Pawlowski J. 2013. Ancient DNA complements microfossil record in deep-sea subsurface sediments. Biol Lett. 9(4):20130283.
  • Li S, Xiao X, Yin X, Wang F. 2006. Bacterial community along a historic lake sediment core of Ardley Island, West Antarctica. Extremophiles. 10(5):461–467.
  • Malbrouck C, Kestemont P. 2006. Effects of microcystins on fish. Environ Toxicol Chem. 25(1):72–86.
  • Manning PG, Prepas EE, Serediak MS. 1999. Pyrite and vivianite intervals in the bottom sediments of eutrophic Baptiste Lake, Alberta. Can Minerologist. 37:593–601.
  • Martínez de la Escalera G, Antoniades D, Bonilla S, Piccini C. 2014. Application of ancient DNA to the reconstruction of past microbial assemblages and for the detection of toxic cyanobacteria in subtropical freshwater ecosystems. Mol Ecol. 23(23):5791–5802.
  • Miller MA, Kudela RM, Mekebri A, Crane D, Oates SC, Tinker MT, Staedler M, Miller WA, Toy-Choutka S, Dominik C, et al. 2010. Evidence for a novel marine harmful algal bloom: cyanotoxin (microcystin) transfer from land to sea otters. PLoS One. 5(9):e12576.
  • Mitchell P, Prepas EE. 1990. Atlas of Alberta lakes. Edmonton, AB: University of Alberta Press.
  • Mohamed ZA, El-Sharouny HM, Ali WSM. 2006. Microcystin production in benthic mats of cyanobacteria in the Nile River and irrigation canals, Egypt. Toxicon. 47(5):584–590.
  • 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(21):6472–6482.
  • Neilan BA, Dittmann E, Rouhiainen L, Bass RA, Schaub V, Sivonen K, Börner T. 1999. Nonribosomal peptide synthesis and toxigenicity of cyanobacteria. J Bacteriol. 181(13):4089–4097.
  • Nübel U, Garcia-Pichel F, Muyzer G. 1997. PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl Environ Microbiol. 63(8):3327–3332.
  • Paerl HW, Huisman J. 2008. Climate. Blooms like it hot. Science. 320(5872):57–58.
  • Pal S, Gregory-Eaves I, Pick FR. 2015. Temporal trends in cyanobacteria revealed through DNA and pigment analyses of temperate lake sediment cores. J Paleolimnol. 54(1):87–101.
  • Paterson AM, Rühland KM, Anstey CV, Smol JP. 2017. Climate as a driver of increasing algal production in Lake of the Woods, Ontario, Canada. Lake. Reserv Manag. 33403–414.
  • Pennington W, Tutin TG, Cambray RS, Fisher EM. 1973. Observations on lake sediments using fallout 137 Cs as a tracer. Nature. 242(5396):324–326.
  • Pick FR. 2016. Blooming algae: a Canadian perspective on the rise of toxic cyanobacteria. Can J Fish Aquat Sci. 73(7):1149–1158.
  • Pimentel JSM, Giani A. 2013. Estimating toxic cyanobacteria in a Brazilian reservoir by quantitative real-time PCR, based on the microcystin synthetase D gene. J Appl Phycol. 25(5):1545–1554.
  • Poulain AJ, Aris-Brosou S, Blais JM, Brazeau M, Keller W, Paterson AM. 2015. Microbial DNA records historical delivery of anthropogenic mercury. Isme J. 9(12):2541–2550.
  • R Core Team. 2013. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.
  • Rajaniemi P, Hrouzek P, Kaštovská K, Willame R, Rantala A, Hoffmann L, Komárek J, Sivonen K. 2005. Phylogenetic and morphological evaluation of the genera Anabaena, Aphanizomenon, Trichormus and Nostoc (Nostocales, Cyanobacteria). Int J Syst Evol Microbiol. 55(Pt 1):11–26.
  • Räsänen J, Kauppila T, Vuorio K. 2006. Sediment and phytoplankton records of the cyanobacterial genus Anabaena in boreal Lake Pyhäjärvi. Hydrobiologia. 568(1):455–465.
  • Rinta-Kanto JM, Ouellette AJA, Boyer GL, Twiss MR, Bridgeman TB, Wilhelm SW. 2005. Quantification of Toxic Microcystis spp. during the 2003 and 2004 blooms in Western Lake Erie using Quantitative Real-Time PCR. Environ Sci Technol. 39(11):4198–4205.
  • Rühland KM, Paterson AM, Hargan K, Jenkin A, Clark BJ, Smol JP. 2010. Reorganization of algal communities in the Lake of the Woods (Ontario, Canada) in response to turn-of-the-century damming and recent warming. Limnol Oceanogr. 55:2433–2451.
  • Rühland KM, Paterson AM, Smol JP. 2015. Lake diatom responses to warming: reviewing the evidence. J Paleolimnol. 54(1):1–35.
  • Savichtcheva O, Debroas D, Kurmayer R, Villar C, Jenny JP, Arnaud F, Perga ME, Domaizon I. 2011. Quantitative PCR enumeration of total/toxic Planktothrix rubescens and total cyanobacteria in preserved DNA isolated from lake sediments. Appl Environ Microbiol. 77(24):8744–8753.
  • Schirrmeister BE, Anisimova M, Bagheri HC, Dalquen DA. 2012. Gene copy number variation and its significance in cyanobacteria phylogeny. Mol Biol Evol. 121586–1591.
  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, et al. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 75(23):7537–7541.
  • Shokralla S, Spall JL, Gibson JF, Hajibabaei M. 2012. Next-generation sequencing technologies for environmental DNA research. Mol Ecol. 21(8):1794–1805.
  • Simpson GL. 2016. Permute: functions for generating restricted permutations of data. R package version 0.9-4.Available from: https://CRAN.R-project.org/package=permute
  • Smol JP. 2008. Pollution of lakes and rivers: a paleoenvironmental perspective. New York, NY: Blackwell Pub.
  • Smol JP, Wolfe AP, Birks HJB, Douglas MSV, Jones VJ, Korhola A, Pienitz R, Ruhland K, Sorvari S, Antoniades D, et al. 2005. Climate-driven regime shifts in the biological communities of arctic lakes. PNAS. 102(12):4397–4402.
  • Stoeva MK, Aris-Brosou S, Chételat J, Hintelmann H, Pelletier P, Poulain AJ. 2014. Microbial community structure in lake and wetland sediments from a high arctic polar desert revealed by targeted transcriptomics. PLoS One. 9(3):e89531.
  • Sun D-L, Jiang X, Wu QL, Zhou N-Y. 2013. Intragenomic heterogeneity of 16S rRNA genes causes overestimation of prokaryotic diversity. Appl Environ Microbiol. 79(19):5962–5969.
  • Taranu ZE, Gregory-Eaves I, Leavitt PR, Bunting L, Buchaca T, Catalan J, Domaizon I, Guilizzoni P, Lami A, McGowan S, et al. 2015. Acceleration of cyanobacterial dominance in North temperate-subarctic lakes during the Anthropocene. Ecol Lett. 18(4):375–384.
  • Taylor S, Wakem M, Dijkman G, Alsarraj M, Nguyen M. 2010. A practical approach to RT-qPCR-Publishing data that conform to the MIQE guidelines. Methods. 50(4):S1–S5.
  • Tillett D, Dittmann E, Erhard M, von Döhren H, Börner T, Neilan BA. 2000. Structural organization of microcystin biosynthesis in Microcystis aeruginosa PCC7806: an integrated peptide-polyketide synthetase system. Chem. Biol. 7(10):753–764.
  • van Geel B, Mur LR, Ralska-Jasiewiczowa M, Goslar T. 1994. Fossil akinetes of Aphanizomenon and Anabaena as indicators for medieval phosphate-eutrophication of Lake Gosciaz (Central Poland). Rev Palaeobot Palynol. 83(1–3):97–105.
  • 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(16):5261–5267.
  • Winter JG, DeSellas AM, Fletcher R, Heintsch L, Morley A, Nakamoto L, Utsumi K. 2011. Algal blooms in Ontario, Canada: Increases in reports since 1994. Lake Reserv Manag. 27(2):107–114.
  • Ye W, Tan J, Liu X, Lin S, Pan J, Li D, Yang H. 2011. Temporal variability of cyanobacterial populations in the water and sediment samples of Lake Taihu as determined by DGGE and real-time PCR. Harmful Algae. 10(5):472–479.
  • Yuan M, Carmichael WW, Hilborn ED. 2006. Microcystin analysis in human sera and liver from human fatalities in Caruaru, Brazil 1996. Toxicon. 48(6):627–640.
  • Zastepa A, Taranu ZE, Kimpe LE, Blais JM, Gregory-Eaves I, Zurawell RW, Pick FR. 2017a. Reconstructing a long-term record of microcystins from the analysis of lake sediments. Sci Total Environ. 579:893–901.
  • Zastepa A, Pick FR, Blais JM. 2017b. Distribution and flux of microcystin congeners in lake sediments. Lake Reserv Manag. 33(4):444–451.
  • Zastepa A, Pick FR, Blais JM, Saleem A. 2015. Analysis of intracellular and extracellular microcystin variants in sediments and pore waters by accelerated solvent extraction and high performance liquid chromatography-tandem mass spectrometry. Analytica Chimica Acta 872:26–34.
  • Zurawell R, Kotak B, Prepas EE. 1999. Influence of lake trophic status on the occurrence of microcystin-LR in the tissue of pulmonate snails. Freshwater Biol. 42(4):707–718.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.