LIMNOLOGY AND OCEANOGRAPHY To aU ee bloom: =e cyanobacteria and FTldiley) ere Cicer ile ( Sylvia Bonilla’ and Frances R. Pick? ree Mice Meter Leute MU ECR MEN etal MU (tENg Poca rsimecltRy ? Department of Biology, University of Ottawa, Canada ie ile aaa Ol (ole c Re) CelerraPeer tons Freshwater bloom-forming cyanobacteria Cyanobacterial traits that contribute to dominance and bloom formation Cyanotoxins Cyanobacteria and environmental factors Anthropogenic factors and climate change Detection, early warning and monitoring Research avenues Class activities Summary Peat ON ere aad+ Prokaryotes that evolved during the Precambrian (~2.7 Ga) and perform oxygenic photosynthesis. * Critical during early evolution of the Earth: created the present oxygenic atmosphere. Ancient cyanobacterial mats (Stromatolites), 500 million years ald, from Greenland. What is their contribution to global biomass? > 1000 million metric tons (101° g) of wet biomass. (Humans: 350 million metric tons, wet biomass) een’ CORP ce aC ON ere aadasic questions = z.=™ CS eS 6S > What do cyanobacteria look like? * Among the smallest and largest species of phytoplankton. Large colonies (Microcystis, up to ~5mm diam) Growth rate: ~ 0.3 day? Picocyanobacteria =" | (Synechoccocus, 0.6 um diam) Growth rate: ~ 2day! (ohso:B. Crema Equivalent: Soccer ball Ground cayenne PS eye ara Peer tons Peer eeeer csWhat do cyanobacteria look like? + Levels of biological organization and complexity. a Unicellular Colonial Filamentous Filamentous+ (specialized cells, (Photos: 1: L Vide: 2 one 4: 8. Haskonseon; 2:8. Clrke) ramifications) een’ PN ler edJe OL = ‘A _=™ = ~ = Where are eet + Any habitat with light: ice, deserts, soil, but especially aquatic Ls oe ecosystems. ani «In freshwater: high - 7 e species diversity, blooms. + Also in symbiosis with other organisms. Se. (eto.:F Pet Pink fishing hole in Outaouais lake, Canada, due to cyanobacteria rich in phycoerythrin pigment. Bonilla & Pick Peat ON ere aadBasic questions What is a bloom? + Visible increase in phytoplankton biomass. * Can last for days to months or become permanent. * Biomass accumulation is highly variable (~ 50 pg L" chl a to mg in scums). eee) Cyanobacterial bloom, Jacarepagua lagoon, Brazil Cee acd CCR aC oy PN ler edStratification c E = 3 8 = g s = 6 > 2 a S & a Peer tons Accumulate (or Accumulate semi-accumulate) \ at depth at surface Disperse throughout lose on Ofer & Gant, 2000: Reynds 1884, 1899, 904) ASLO e-lecturesBlo om-forming cy ole Unicellular, colonial* Chroococcales Oscillatoriales Filament Nostocales Filament rot] calls CEST Accumulative No Dispersive Accumulative or dispersive Heterocytes (Atmospheric N, fixation) Akinetes aT SCE ute) Microcystis Sphaerocavum Woronichinia Planktothrix Limnothrix Cylindrospermopsis Dolichospermum Aphanizomenon Gloeotrichia *Microcystis, the most common bloom-forming cyanobacterial genus in freshwaters in the world, with largest biomass in blooms (mg wet weight). Peer tons Pees Ty PS eye araeRe A Trl yt Recall} Peer tons Pees Ty ASLO e-lectures> _ Eye of a cyanobaci Tous EU treet) (notice the white boat id the dark line Lehr) Fs, Peer tons Peer eeeer cs UNS ey eedTraits contributing to dominance and bloom formation: 1. Peer tons Large size of colonies or filaments . Tolerance of extremes in solar radiation . Particular pigments . Nutrient storage . N, fixation . Buoyancy regulation through gas vacuoles . Benthic resting stages . Toxins and more... Peat PN ler ed+ Large storage capacity for N, P. + Gas vacuoles enable vertical migrations (optimizing both light and nutrient capture). + Low grazing losses (most planktonic grazers prefer particles < 35 um). (rae Aamo) Gloeotrichia echinulata colonies comprised of filaments can be visible to naked eye (~ mm in diameter appearing as fuzzy balls in surface waters) Microcystis colonies form surface scums at La Plata River estuary, Uruguay. eer iar Peary ON ere aad* Major light harvesting pigments: Phycobilins (allophycocyanin, phycocyanin and phycoerythrin). lke 8 ort Picocyanobacteria cultures rich in phycoerythrin (left) and phycocyanin (right). (culture collection of WF. Vincent). Peer tons @ sopivcocyaniny If Prycocyann J Prvcoerv tren A) General structure of phycobilisomes (PHYS). B) PHYS are located on the surface of thylakoids. Gylinder in green: PS | & Il with chlorophyll a; in grey: thylakoid. ASLO e-lectures* Phycobilins: Capture light at intermediate wavelengths (~562 to ~650 nm). | Chlorophyll b . Phycoerythrin Phi ,| Absorption spectra of major aucoganin pigments in algae and cyanobacteria. Phycoerythrin and phycocyanin are major pigments in cyanobacteria. (Chlorophyll b only present in some cyanobacteria). “350 300 350 400 450 $00 550 600 650 700 Violet Blue Green’ Yellow Red Wavelength (nm) (Fron: hin cas lariohed-mwicanc/ANATOMICHS, Absorstvelarliniha009 ir) een’ Peary ON ere aadPlanktothrix bloom rich in phycoerythrin, in Central Ontario lake, Canada. phycocyanin from a scenescent Microcystis bloom at the shore of areservoir, Uruguay. een’ CORP ce aC ON ere aadigh eele Polyphosphate granules Polyphosphate granules (bright yellow dots) in a filament of Planktothrix agardhii (x 1000). Petar Anabaena variabilis with cyanophycin [C] granules, TEM image (modified from Ziegler et al. 2001) Pees Ty PS eye araal ee Tee ee Successful with: 1. No nutrient limitation: Nutrient uptake and growth are temporally coupled. tial yey High nutrient concentration tee et . Nutrient limitation: 25* irre Acquisition and storage of 2s reece | t nutrients (e.g polyphosphate 32 a 28 storage granules): Nutrient uptake and growth are temporally uncoupled. Bh Nutrient uptake Phytoplankton growth t time (based Aut a 2011, ond Asriot 8 Sona, 2012) ASLO e-lectures Peer tors Peer eeeer csHeterocyte (H): site of N, fixation in Nostocales thick cell walls pale and uniform content due to absence of PSII and less photosynthetic pigments (leading to low internal [O,]) oe tiaonasneee — nitrogenase enzyme Dolichospermum (Anabaena): a common bloom- forming, diazotrophic, filamentous cyanobacterium; top (x200) and bottom (x1000). een’ PN ler edFactors regulati 7 z availability Solar energy \ L r. availability DIN: Low N/P from Dissolved inorganic N recycled nutrients, (NH,*, NO,") la’ high P loading rdf rom Howarth tal, 198) Petar 4 ASLO e-lectures+ Akinete (A): specialized dormancy cell (resting stage) in Nostocales. + Thick cell wall, rich in nutrients , + Shape, location on filament is characteristic of species. + Can detach and persist in sediments/soil to germinate when conditions improve. Dolichospermum with large akinete (A) een’ CORP ce aC ON ere aadGas vesicles = Pi eiiey as Eee Microcystis cells filled with vacuola TEM image of a cyanobacterial cell full of (grouped gas vesicles) (x1 000) gas vesicles (GS) (hexagonal structures). (From Walsby, 1974). Bonilla & Pick Peer eeeer cs ASLO e-Peer tons Balance carbohydrate/buoyancy regulated by nutrients and light * + carbohydrates : ++ polyphosphate + + Photosynthesis granules i + Less ballast effect — lower density BALLAST * Flotation (gas vesicles) 3 Metabolic 2 processes sless carbohydrates due to respiration Seesen ber 27, bine tt, 10 Rin Se, 188 Peat PN ler ed= Scums: high accumulation of biomass at the surface. Loss of buoyancy regulation. Time “1 —_, ws? eee ue at the surface due to gas vacuol oh: 8a Vertical migration: + From < 1 mm to ~ 10 m per day. Ee + Depends on species and size: 10,000 cell L" 100,000,000 cell L" smaller organisms migrate less. Change in cell density at surface Peer tons 0. ASLO e-lecturesFunctions: 1. Formation of colonies. . Protection against desiccation. . Protection against UV radiation. . Nutrient uptake (e.g. Fe). . Filter against contaminants (e.g. heavy metals). . Decrease organism density. 7. Decrease predation pressure (predator avoidance, low digestibility). Cyanobacteria at 1000x with black ink to highlight the transparent mucilage. (top: Dalichospermum, and bottom: Microcystis) nRWN a Bonilla & Pick Peat ON ere aada —. as Cec c o 5 a Molecular Weight Chemical structure Number of variants Toxin type LDsy (ug kg" b.w.) Peer tons Microcystins 909-1115 > 200 Hepatotoxic 50->1200 Anatoxins Saxitoxins Neurotoxic — Neurotoxic 10 Cylindro- spermopsins 415 ats oft “Fo ow uy on cel “eit Cytotoxic 2100 ASLO e-lecturesPhotos: 1: Cylindrospermopsis raciborksil, B. Cremella; 2: Radiooystis sp., M.C. Pérez; 3: Dolichospermum sp. 8. Haakonsson; 4: Woronichinia sp, F. Pick; 5: Plankiothrix sp, B. Clarke; 6: Dolichospermum lemmenmanil F. Pick). Peer tons Peer eeeer cs PX eye acaCee em te rh = >» In 1996, microcystins caused 60 deaths when contaminated reservoir water was used at a dialysis clinic (Caruaru, Brazil). Several patients had visual disturbances, nausea, vomiting, and muscle weakness. ™ Patients affected 5 Deaths 19.5 pg L” microcystin in dialysis water een’ CORP ce aC PN ler edElith< * Toxins can be transferred to higher trophic levels. * Persistence and bioaccumulation of microcystins (MCs). * MCs: the most common cyanotoxins. In 2010, dietary exposure to MCs from an upstream lake caused ~ 21 sea otter deaths (an endangered species) near Monterey, California, USA. (miller et al. 2010) Peer tons Peer eeeer cs PX eye acaBera) te _ ~~ Oo * BMAA: non protein amino acid (beta-N-methylamino- lia L-alanine). NH ‘OH Agent of neuro-degeneration? S Link with Amyotrophic Lateral Sclerosis? Through food web- bioaccumulation. ¢ Retinoic acids (RAs) Cyanobacterial blooms produce RAs and RA mimics, highly teratogenic leading to developmental deformities. Frog (Hyla regilla) with two extra hind limbs (om Balin & Jean, 203) Cooter PN ler ed+ Defense against grazing + Allelochemicals + Infochemicals and quorum sensing 0=3=0 + Metal acquisition and storage + Reserves of nitrogen + Counter environmental stress 9 Bonilla & Pick Peer eeeer cs ON ere aadSU ~~ Fi _ y Geosmin and 2-methylisoborneol (2MIB): volatile tertiary alcohols, smell of damp or muddy soil * Very persistent, negative effect on water quality. * Very low or no toxicity to humans. * No correlation between presence of toxins and taste and odor compounds. x 4: ose ps edsowea'/20181 0th * Humans: best “detectors” (smell threshold < 10 ng L"). een’ PN ler edSurvival and growth: + To optimize acquisition of resources (light and nutrients). * To minimize loss by predation and sedimentation. ES Dissolved nutrients in More planktivorous the water column fish Transparency Sedimentation out of More predators the euphotic zone (zooplankton) Low residence time Competition with algae (wash out) or plants for resources Allelopathy Peer tons Peer eeeer csResources: Light How is the light environment for phytoplankton? Z,,: euphotic zone Zi: Mixing zone 25, Zi 2, <2, Cyanobacteria Microcystis aeruginosa _—_Cylindrospermopsis raciborskii bloom-forming Radiocystis Planktothrix agardhii genera or species Dolichospermum Limnothrix Peer tors Peer eeeer csCCE te =, Se Macronutrients Cyanobacterial strategies for coping (> 0.1 % dry weight) | with limiting conditions Carbon (C) Can use bicarbonate (HCO, ). Have highly efficient CO, concentrating mechanisms (CCM). Oxygen (O) No limitation Hydrogen (H) No limitation z = 4 = < z Nitrogen (N) Some can fix atmospheric Nitrogen (N) if inorganic dissolved forms are limiting. Plus storage capacity. Very efficient at the acquisition of phosphorus. Plus storage capacity. Phosphorus (P) een’ CORP ce aC PN ler edCyanobacterial biomass (biovolume) predicted by total nitrogen and temperature. Survey (US National Lake Assessment, n = 1147) Nitrogen Temperature © ‘Natural lakes ® Reservoirs 3 3 3 3 i i 5 g, o co &. z og total nitrogen (Lo) mean water colurin temperature (°C) (rom Beau tl, 2013 Cee acd eae ON ere aadCa _ i 5 : e z g g Peer tons ber He Latitudinal grad : ~ » Latitudinal gradients affect phytoplankton biomass \ rn annual cycles. : * Light, temperature and precipitation regime > big regional scale factors. Cold temperate ‘Subtropical Temperate lake with ice cover in winter (top panel), tropical lake (bottom) with Tenia dry (sunny) and wet (rainy) seasons. YN Cya: most probable period for cyanobacterial growth. Season ASLO e-lectures> Fd is — — " A t Ws rerann om Raye, 1984) inelnpat C More nutrients O: Output More phytoplankton : R: Recycling Se: Sedimentation C b: . B: Phytoplankton biomass yanobacteria ASLO e-lecturesMTree iret ite thd Ecosystem level experiment: Lake 226 fertilization (Schindler et al., 1971, 1973) aire R Ua) ~ Carbon & Nitrogen isnt Pao nln) Strong dominance of Lake 226 from Carbon, Nitrogen diazotrophic Aph i 9 ee Peer tons Peer eeeer cs ASLO e-Dominant size classes Microphytoplankton Preophytoplankton Total phytoplankton biomass (%) 10 20 > as Total phosphorus (ug I?) Total phosphorus (ua r*) Veonkar 20) [Fon Waten tat 097) More nutrients > more large cyanobacteria Perret ASLO e-lecturesConstruction of dams on rivers: creation of artificial lakes (reservoirs). (c) y=-0.15L0(x) + 1.26 R= 0.012 (d) YE-1.55Ln(x) +40 (ug L-) 5 : 3 4 nd & a 3 3 2 = = Microcystis biovolume 15 20 3 Water flushing (m? s~1) Water flushing (m® s~!) LCi [elate (hom Romo eta, 2014) Increase in residence time > More nutrients > More cyanobacteria ASLO e-lectures+ Can reach water bodies from agricultural land use. * Can lead to unpredictable changes on phytoplankton. * A potential source of nutrients. * Cyanobacteria can be more tolerant than algae. PerETELCY Glyphosate: herbicide Black: control Pale grey: 1 pM P Dark Grey: 1 uM Glyphosate *p>0.05 Pronktothri spp. Merocystis spp. Auloeosoira spp. Diatom (rm Saxton etal. 2011), Cyanobacteria ASLO e-lecturestried EE ate chi a tt warming Climate change: rising rene _ bi KS), temperatures, weather extremes SEs Weg genni als (in precipitation and storms) MORE MORE & ie Srgenic carbon nutans Vv MORE cyanobacteria HIGHER algal biomass GREATER: turbidity & hee MORE sedimentation _ absorption of organic matter Se MORE SBe Less, piration oxygen in —> Carbon sequestration routes bottom wate —> Carbon emission routes —> Other climate effects ~~ > Precipitation may lead to more Item oss tal, 2081), or less carbon loading PS eye ara Pees Ty Peer tonsThe case of Cylindrospermopsis raciborskii © C. raciborskii Mb © 2009 wrw.cutine-world-map.com Me + Diazotrophic filamentous cyanobacteria. * Can produce potent toxins (cylindrospermopsin or saxitoxin). * Has high physiological plasticity. + Dispersive blooms: increasing distribution. * From warm to temperate climates? Bonilla & Pick Peer eeeer cs ON ere aadDecline in water quality 1. Smell, color and taste in the water. . Anoxic water in the bottom. 3. Health threats: cyanotoxins. . Lower biodiversity. Petar Panacea c ian eect eT Senescent bloom, Ontario lake, pe (phot. Zsa} PS eye araCyanotoxins: Threaten or limit water use (e.g. drinking, recreation, livestock) Toledo, Ohio, without safe tap water Water treatment plant finds samples with mierosystin, produet of Lake Ere alga rans Cee eke eee een’ Peat DN lerPREVENTION RESTORATION Integration of: research, management and citizen engagement Peer tons Peer eeeer csiT EY ey a a advisory limits Cyanobacteria in drinking and recreational waters Levels WHO Cyanobacteria biomass Drinking | Recreational Biovolume Cells Chla water water far | q WHO mm L cell mL pg L nati soe | 1 Canada MC-LR Alert1 | Australia 20.000 | 10 Total MC Alert 2 Guide 2 100.000 | 50 | n . . Low 2-4 inode ton Chow & Bara, 198 Moderate 5-20 Quantita indicators: number of cells, biovolume, phytoplankton chlorophyll a High ez) trom Chane & Barwon 1999; Chen, 2006, 2012) Peer tons Peer eeeer csParticulate MC ug 1 Bonilla & 9 16 25 P. agardhii biovolume mm I Is this bloom toxic? 70 WHO, Guide 2 00 30 0 » WHO limit, high a adverse effects 0 Chlorophyll (ug/L) La Plata River, Uruguay. (rom Pree et, 2082) Lakes of northem Germany. (om Dotan ett, 2012) Pees Ty ASLO e-lecturesApproach Objective Policies Reduce usage and external loading of N and P (fertilizers, sewage etc.) Chemical Precipitate nutrients and sequester in sediments (alum, iron chloride treatments) Physical Mixing/aeration; removal of sediments; sonication Bio-manipulation | Introduction/removal of a keystone species to trigger reduction in phytoplankton On-site BMPs Green infrastructure (vegetative buffers, constructed wetlands) Aerator for a lake on Salt Spring Island, Canada eer iar ON ere aadBiology + What is the physiological function (if any) of cyanotoxins? + To what extent do cyanotoxins impact food webs? + Emerging metabolites with toxicological/environmental effects. Organism-environment Should N also be regulated to control cyanobacteria in freshwater? Or can nitrogen fixation always keep pace with P loading? Invasive species or changing environmental conditions? Methods for rapid detection of cyanobacteria and cyanotoxins. een’ CORP ce aC ON ere aadterre et Ned New methods to detect and monitor cyanobacteria in the field: Three scales: 1. From inside the cell: Immunofluorescence-labelling techniques, Molecular tools 3. From outside the ecosystem: Remote sensing, Spectroscopy 2. From outside the cell : Invivo pigment fluorescence Peer tons Pees TyExamples: 1. From inside the cell: Immunofluorescence-labelling techniques | acral Molecular tools 3 meyD,., (x 10° copies mL") Polyclonal antibodies against saxitoxin with catalyzed reporter deposition. Detection of microcystin-producing Arrows: saxitoxin (green) within the cells. cyanobacteria with Quantitative PCR Chlorophyll a: red. (x 600). (gene: mcyD) in a lake. (Gm Peni et 2013) rom Fon al, 2010) Peer tons Pema te PX eye aca* Examples: 2. From outside the cell: In vivo pigment fluorescence ° ‘2000 ‘4000 ‘6000 Cyanobacteria (cells/ml) Phycocyanin fluorescence vs. cyanobacterial abundance (up to 6000 and up to 2000 cells, insert). (om Geog et 2007 Petar Pees Ty ” 3. From outside the ecosystem: Remote sensing Images with time, Lake Erie. Colors show bloom intensity. (em Sumer al, 2012) PS eye ara1 KK. n supplementary materials you will find class activities Ee Develop your own bloom 3 weeks Medium to high Illustrate the effects of organism 3-4 hours Low size on sedimentation and gas vacuoles in buoyancy regulation. Universidad do le Raptlca, Uruguy, 2014) Peer tons Peer eeeer cs PX eye aca+ Among the most ancient organisms on Earth, currently very successful. + Freshwater blooms have ecosystem level impacts. - Produce several metabolites (e.g. cyanotoxins) that affect water quality, wildlife and human health. + Nutrient loading and climate change will more than likely increase incidence and severity of cyanobacterial blooms. + More experts in cyanobacteria and cyanotoxins will be needed in the future to manage surface waters. een’ PN ler edTd Acknowledgements Research funding support from the Universidad de la Republica and Agencia Nacional de Investigacién e Innovacién (ANII) of Uruguay (S. Bonilla), and from the Natural Sciences and Engineering Research Council of Canada (F. Pick). We thank ASLO reviewers and editors for their suggestions for improvement of content and presentation. 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Bonilla & Pick Peer eeeer cs EN ere aadCopyright ©2017 by The Association for the Sciences of Limnology and Oceanography (ASLO) Published by John Wiley & Sons, Inc. Sylvia Bonilla and Frances R. Pick Freshwater Bloom-forming Cyanobacteria and Anthropogenic Change doi:10.1002/loe2.10006 e-Lecture received June 2016; accepted August 2017 For more information, please visit the ASLO e-Lectures page at http://onlinelibrary.wiley.com/journal/10.1002/(ISSN)2164-0254 een’ CORP ce aC ON ere aad