Trophic state and geographic gradients influence planktonic cyanobacterial diversity and distribution in New Zealand lakes

&NA; Cyanobacteria are commonly associated with eutrophic lakes, where they often form blooms and produce toxins. However, they are a ubiquitous component of phytoplankton in lakes of widely varying trophic status. We hypothesised that cyanobacterial diversity would vary among lakes of differing trophic status, but that the relative importance of geographical and hydromorphological characteristics driving these patterns would differ across trophic groups. DNA from 143 New Zealand lakes that spanned a range of geographic, hydromorphological and trophic gradients was analysed using automated rRNA intergenic spacer analysis and screened for genes involved in cyanotoxin production. Statistical analysis revealed significant delineation among cyanobacterial communities from different trophic classes. Multivariate regression indicated that geographical features (latitude, longitude and altitude) were significant in driving cyanobacterial community structure; however, partitioning of their effects varied among trophic categories. High‐throughput sequencing was undertaken on selected samples to investigate their taxonomic composition. The most abundant and diverse (71 operational taxonomic units) taxon across all lake types was the picocyanobacteria genus Synechococcus. Cyanotoxins (microcystins n = 23, anatoxins n = 1) were only detected in eutrophic lowland lakes. Collectively, these data infer that increasing eutrophication of lakes will have broad‐scale impacts on planktonic cyanobacteria diversity and the prevalence of cyanotoxins.

[1]  R. Zurawell,et al.  Predicting cyanobacterial dynamics in the face of global change: the importance of scale and environmental context , 2012 .

[2]  C. Callieri,et al.  Picocyanobacterial community structure and space-time dynamics in the subalpine Lake Maggiore (N. Italy) , 2012 .

[3]  F. Hildebrand,et al.  Diversity of toxin and non-toxin containing cyanobacterial mats of meltwater ponds on the Antarctic Peninsula: a pyrosequencing approach , 2014, Antarctic Science.

[4]  D. Penney Biodiversity in Space and Time , 2013 .

[5]  A. Kerkhoff,et al.  Microbes on mountainsides: Contrasting elevational patterns of bacterial and plant diversity , 2008, Proceedings of the National Academy of Sciences.

[6]  David P. Hamilton,et al.  Recent invader or indicator of environmental change? A phylogenetic and ecological study of Cylindrospermopsis raciborskii in New Zealand , 2014 .

[7]  D. Dietrich,et al.  Potent toxins in Arctic environments--presence of saxitoxins and an unusual microcystin variant in Arctic freshwater ecosystems. , 2013, Chemico-biological interactions.

[8]  David P. Hamilton,et al.  High Levels of Structural Diversity Observed in Microcystins from Microcystis CAWBG11 and Characterization of Six New Microcystin Congeners , 2014, Marine drugs.

[9]  A. Eiler,et al.  Unveiling Distribution Patterns of Freshwater Phytoplankton by a Next Generation Sequencing Based Approach , 2013, PloS one.

[10]  J. Stockner,et al.  Picoplankton and other non-bloom forming Cyanobacteria in lakes , 2000 .

[11]  Raymond N. Gorley,et al.  PERMANOVA+ for PRIMER. Guide to software and statistical methods , 2008 .

[12]  D. Cowan,et al.  Sources of edaphic cyanobacterial diversity in the Dry Valleys of Eastern Antarctica , 2008, The ISME Journal.

[13]  Nancy Knowlton,et al.  Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. , 2007, Ecology letters.

[14]  Martin Hartmann,et al.  Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities , 2009, Applied and Environmental Microbiology.

[15]  S. Wood,et al.  Consumption of benthic cyanobacterial mats and nodularin-R accumulation in freshwater crayfish (Paranephrops planifrons) in Lake Tikitapu (Rotorua, New Zealand) , 2012 .

[16]  E. Rizzi,et al.  Anatoxin-a Synthetase Gene Cluster of the Cyanobacterium Anabaena sp. Strain 37 and Molecular Methods To Detect Potential Producers , 2011, Applied and Environmental Microbiology.

[17]  David P. Hamilton,et al.  Low dissolved inorganic nitrogen and increased heterocyte frequency: precursors to Anabaena planktonica blooms in a temperate, eutrophic reservoir , 2010, Journal of Plankton Research.

[18]  H. Paerl,et al.  A review of the global ecology, genomics, and biogeography of the toxic cyanobacterium, Microcystis spp. , 2016, Harmful algae.

[19]  G. Codd,et al.  Cyanobacterial toxins: risk management for health protection. , 2005, Toxicology and applied pharmacology.

[20]  P. Buscarinu,et al.  Effects of trophic status on microcystin production and the dominance of cyanobacteria in the phytoplankton assemblage of Mediterranean reservoirs , 2015, Scientific Reports.

[21]  Sven Becker,et al.  Seasonal and habitat-related distribution pattern of Synechococcus genotypes in Lake Constance. , 2007, FEMS microbiology ecology.

[22]  B. Whitton Ecology of Cyanobacteria II , 2012, Springer Netherlands.

[23]  T. Börner,et al.  Abundance of active and inactive microcystin genotypes in populations of the toxic cyanobacterium Planktothrix spp. , 2004, Environmental microbiology.

[24]  S. Wood,et al.  Brown trout (Salmo trutta) removal by rotenone alters zooplankton and phytoplankton community composition in a shallow mesotrophic reservoir , 2015 .

[25]  S. Wood,et al.  Survey of Scytonema (Cyanobacteria) and associated saxitoxins in the littoral zone of recreational lakes in Canterbury, New Zealand , 2012 .

[26]  Brian H. McArdle,et al.  FITTING MULTIVARIATE MODELS TO COMMUNITY DATA: A COMMENT ON DISTANCE‐BASED REDUNDANCY ANALYSIS , 2001 .

[27]  C. Bernard,et al.  Design and application of a stratified sampling strategy to study the regional distribution of cyanobacteria (Ile-de-France, France). , 2008, Water research.

[28]  M. Schallenberg,et al.  Tests of autotrophic picoplankton as early indicators of nutrient enrichment in an ultra-oligotrophic lake , 2001 .

[29]  F. Garcia-Pichel,et al.  Polyphasic characterization of benthic, moderately halophilic, moderately thermophilic cyanobacteria with very thin trichomes and the proposal of Halomicronemaexcentricum gen. nov., sp. nov. , 2002, Archives of Microbiology.

[30]  R. Henrik Nilsson,et al.  Taxonomic Reliability of DNA Sequences in Public Sequence Databases: A Fungal Perspective , 2006, PloS one.

[31]  James H Brown,et al.  A latitudinal diversity gradient in planktonic marine bacteria , 2008, Proceedings of the National Academy of Sciences.

[32]  Elena Litchman,et al.  Large-scale biodiversity patterns in freshwater phytoplankton. , 2011, Ecology.

[33]  J. Downing,et al.  Predicting cyanobacteria dominance in lakes , 2001 .

[34]  A. Jungblut,et al.  Molecular identification and evolution of the cyclic peptide hepatotoxins, microcystin and nodularin, synthetase genes in three orders of cyanobacteria , 2006, Archives of Microbiology.

[35]  Eoin L. Brodie,et al.  Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB , 2006, Applied and Environmental Microbiology.

[36]  S. Wood,et al.  Geographically conserved microbiomes of four temperate water tunicates. , 2016, Environmental microbiology reports.

[37]  P. Sánchez‐Baracaldo,et al.  Picocyanobacterial community structure of freshwater lakes and the Baltic Sea revealed by phylogenetic analyses and clade-specific quantitative PCR. , 2008, Microbiology.

[38]  Sven Becker,et al.  Spatio-temporal niche partitioning of closely related picocyanobacteria clades and phycocyanin pigment types in Lake Constance (Germany). , 2012, FEMS microbiology ecology.

[39]  Lisa R. Moore,et al.  Ecotypic variation in phosphorus-acquisition mechanisms within marine picocyanobacteria , 2005 .

[40]  J. Stockner,et al.  Picoplankton in Six New Zealand Lakes: Abundance in Relation to Season and Trophic State , 1991 .

[41]  C. Reynolds,et al.  The distribution of planktonic Cyanobacteria in Irish lakes in relation to their trophic states , 2000, Hydrobiologia.

[42]  B. Neilan,et al.  Characterization of the Gene Cluster Responsible for Cylindrospermopsin Biosynthesis , 2007, Applied and Environmental Microbiology.

[43]  R. Holt,et al.  Phytoplankton species richness scales consistently from laboratory microcosms to the world's oceans. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[44]  R. Ptáčník,et al.  Regional species pools control community saturation in lake phytoplankton , 2010, Proceedings of the Royal Society B: Biological Sciences.

[45]  S. Wood,et al.  First report of saxitoxin production by a species of the freshwater benthic cyanobacterium, Scytonema Agardh. , 2011, Toxicon : official journal of the International Society on Toxinology.

[46]  Y. Nojiri,et al.  PICOPHYTOPLANKTON BIOMASS IN RELATION TO LAKE TROPHIC STATE AND THE TN:TP RATIO OF LAKE WATER IN JAPAN 1 , 1994 .

[47]  A. Walsby,et al.  Gas vesicles , 1994, Microbiological reviews.

[48]  W. Carmichael,et al.  Toxicity and partial structure of a hepatotoxic peptide produced by the cyanobacterium Nodularia spumigena Mertens emend. L575 from New Zealand , 1988, Applied and Environmental Microbiology.

[49]  S. Wood,et al.  Survey of cyanotoxins in New Zealand water bodies between 2001 and 2004 , 2006 .

[50]  G. Fleming,et al.  Molecular fingerprinting of lacustrian cyanobacterial communities: regional patterns in summer diversity. , 2013, FEMS microbiology ecology.

[51]  David P. Hamilton,et al.  Contrasting cyanobacterial communities and microcystin concentrations in summers with extreme weather events: insights into potential effects of climate change , 2016, Hydrobiologia.

[52]  S. Wood,et al.  First identification of the cylindrospermopsin‐producing cyanobacterium Cylindrospermopsis raciborskii in New Zealand , 2003 .

[53]  Thomas Rohrlack,et al.  Cyanobacteria and Cyanotoxins: The Influence of Nitrogen versus Phosphorus , 2012, PloS one.

[54]  S. Wood,et al.  FIRST REPORT OF THE CYANOTOXIN ANATOXIN‐A FROM APHANIZOMENON ISSATSCHENKOI (CYANOBACTERIA) 1 , 2007 .

[55]  S. Wood,et al.  Development of solid phase adsorption toxin tracking (SPATT) for monitoring anatoxin-a and homoanatoxin-a in river water. , 2011, Chemosphere.

[56]  I. Janse,et al.  High-Resolution Differentiation of Cyanobacteria by Using rRNA-Internal Transcribed Spacer Denaturing Gradient Gel Electrophoresis , 2003, Applied and Environmental Microbiology.

[57]  A. Ballot,et al.  Paralytic Shellfish Poisoning Toxin-Producing Cyanobacterium Aphanizomenon gracile in Northeast Germany , 2010, Applied and Environmental Microbiology.

[58]  David P. Hamilton,et al.  Catchment land use and trophic state impacts on phytoplankton composition: a case study from the Rotorua lakes’ district, New Zealand , 2012, Hydrobiologia.

[59]  H. Paerl,et al.  Blooms Like It Hot , 2008, Science.

[60]  S. Wood,et al.  New Zealand risk management approach for toxic cyanobacteria in drinking water , 2007, Australian and New Zealand journal of public health.

[61]  S. Interlandi,et al.  LIMITING RESOURCES AND THE REGULATION OF DIVERSITY IN PHYTOPLANKTON COMMUNITIES , 2001 .

[62]  David P. Hamilton,et al.  Phytoplankton assemblages in North Island lakes of New Zealand: Is trophic state, mixing, or light climate more important? , 2006 .

[63]  David P. Hamilton,et al.  Phytoplankton succession and the formation of a deep chlorophyll maximum in a hypertrophic volcanic lake , 2015, Hydrobiologia.

[64]  Anas Ghadouani,et al.  Local nutrient regimes determine site-specific environmental triggers of cyanobacterial and microcystin variability in urban lakes , 2014 .

[65]  W. Ludwig,et al.  SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB , 2007, Nucleic acids research.

[66]  M. Beklioğlu,et al.  Climate change impacts on lakes: an integrated ecological perspective based on a multi-faceted approach, with special focus on shallow lakes , 2014 .

[67]  Sven Becker,et al.  Ecosystem-dependent adaptive radiations of picocyanobacteria inferred from 16S rRNA and ITS-1 sequence analysis. , 2003, Microbiology.

[68]  H. R. Tervit,et al.  Maintenance of cyanotoxin production by cryopreserved cyanobacteria in the New Zealand culture collection , 2008 .

[69]  S. Hamilton,et al.  Nitrogen availability increases the toxin quota of a harmful cyanobacterium, Microcystis aeruginosa. , 2014, Water research.

[70]  Pierre Legendre,et al.  DISTANCE‐BASED REDUNDANCY ANALYSIS: TESTING MULTISPECIES RESPONSES IN MULTIFACTORIAL ECOLOGICAL EXPERIMENTS , 1999 .

[71]  James H. Brown,et al.  Global Biodiversity, Biochemical Kinetics, and the Energetic-Equivalence Rule , 2002, Science.

[72]  Louis A. Tremblay,et al.  Molecular genetic tools for environmental monitoring of New Zealand's aquatic habitats, past, present and the future , 2013 .

[73]  Lemian Liu,et al.  Algae community and trophic state of subtropical reservoirs in southeast Fujian, China , 2012, Environmental Science and Pollution Research.

[74]  B. Whitton Ecology of cyanobacteria II : their diversity in space and time , 2012 .

[75]  Eric P. Nawrocki,et al.  An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea , 2011, The ISME Journal.

[76]  S. Dyhrman,et al.  Phosphorus Scavenging in the Unicellular Marine Diazotroph Crocosphaera watsonii , 2006, Applied and Environmental Microbiology.

[77]  S. Wood,et al.  Successional Change in Microbial Communities of Benthic Phormidium-Dominated Biofilms , 2014, Microbial Ecology.

[78]  L. Vörös,et al.  Freshwater picocyanobacteria along a trophic gradient and light quality range , 1998 .

[79]  Lucas J. Stal,et al.  Nitrogen fixation in cyanobacteria , 2008 .

[80]  Rob Knight,et al.  UCHIME improves sensitivity and speed of chimera detection , 2011, Bioinform..