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CY CYANO ANOTOXINS: WHA INS: WHAT THEY ARE THEY ARE AND WHY THEY AND WHY THEY MA MATTER TTER Frank Wilhelm ank Wilhelm fwilhelm@uidaho.edu fwilhelm@uidaho.edu 208-885-72 208-885-7218 ACKNO KNOWLEDGEMENT WLEDGEMENTS Graduat

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CY CYANO ANOTOXINS: WHA INS: WHAT THEY ARE THEY ARE AND WHY THEY AND WHY THEY MA MATTER TTER Frank Wilhelm ank Wilhelm

fwilhelm@uidaho.edu fwilhelm@uidaho.edu 208-885-72 208-885-7218

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SLIDE 2

ACKNO KNOWLEDGEMENT WLEDGEMENTS

  • Graduat

Graduate students (Sarah Burnet, T students (Sarah Burnet, Ted Harris) d Harris)

  • US Arm

US Army Corps, Idaho EPSCoR, and NSF y Corps, Idaho EPSCoR, and NSF

  • Undergraduat

Undergraduate students/f e students/field assistants ield assistants

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SLIDE 3

Limnologist – study of inland water

At UI since 2007

  • teach / research / train graduate students
  • Interests – lake management/surface water

protection/remediation

  • Introduced species

Wide variety of projects

  • Invertebrates (mysids/tadpole shrimp)
  • Didymo (rock snot) mats,
  • Algae in response to watershed inputs (CDA)
  • Cyanobacteria (Willow Creek Reservoir / Fernan)
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SLIDE 4

OUTLINE OUTLINE

  • Cy

Cyanobact anobacteria back ria backgr ground/o

  • und/overvie

iew w

  • To

Toxins

  • Toxins and human health

xins and human health

  • Conditions that pr

Conditions that produce blooms

  • duce blooms
  • Blooms and t

Blooms and toxins xins

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SLIDE 5

CYANOBAC ACTERIA -

  • BAC

ACKG KGROUND

  • Source of our atmosphere approx. 3.5 bya
  • Bacteria / algae characteristics

‐Chlorophyll a, evolve O2 ‐no cellulose in walls, no membrane‐bound

  • rganelles, reproduction via fission, can fix

nitrogen

  • Occur in wide range of habitats and forms
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SLIDE 6

CYANOBAC ACTERIA -

  • BAC

ACKG KGROUND

  • Heterocysts – specialized cells to fix nitrogen
  • Akinetes – resting cells
  • Vacuoles – gas‐filled vesicles to regulate buoyancy
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SLIDE 7

CY CYANOBA ANOBACTERIA – TERIA – WHY DO WE C HY DO WE CARE? RE?

  • Aesthetics (surface scums)
  • Taste and odor issues
  • Use O2 when decomposing
  • Produce suite of potent toxins
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SLIDE 8

CY CYANOBA ANOBACTERIA – TERIA – WHO ARE THE PLA HO ARE THE PLAYERS? ERS?

Anabaena Aphanizomenon Microcystis Lyngbya Gleotrichia Woronichinia

All have been found to occur in Idaho HABs

(Annie – Fannie – Mike)

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SLIDE 9

…and if those names weren’t confusing enough

Recent name changes: Anabaena ‐‐ Dolichospermum Aphanizomenon ‐‐ Chrysosporum

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http://cfb.unh.edu/phycokey/Choices/Cyanobacteria/cyano_ filaments/cyano_unbranched_fil/untapered_filaments/heter

  • cysts/no_visible_sheath/ANABAENA/Anabaena_Image_pag

e.html#pic12

Anabaena (Dolichospermum)

Toxin – Anatoxin, microcystis

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SLIDE 11

Spring bloom of Anabaena (Dolichospermum)

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SLIDE 12

http://cfb.unh.edu/phycokey/Choices/Cyanobacteria/cyano_filaments/cyano_unbranched_fil/taper ed_filaments/APHANIZOMENON/Aphanizomenon_Image_page.html#pic06

Aphanizomenon (Chrysosporum)

Toxin – cylindrospermopsin, saxitoxin‐like

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SLIDE 13

Microcystis

Stores nitrogen – does not fix Toxin – microcystin, anatoxin

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SLIDE 14

lifesciences.napier.ac .uk lifesciences.napier.ac .uk lifesciences.napier.ac .uk

Gleotrichia

Toxin – microcystin LR Takes up P from sediments in early spring

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SLIDE 15

http://cfb.unh.edu/phycokey/Choices/Cyanobacteria/cyano_filaments/cyano_unbranched_ fil/untapered_filaments/no_heterocysts/vis_sheath/LYNGBYA/Lyngbya_Image_page.htm#pi c07

Entwisle et al. Posted at rbgsyd.nsw.gov.au

Lyngbya

Fixes nitrogen without heterocysts – mainly at night when P/S is absent

Toxin – cylindrospermopsin, saxitoxin‐like

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SLIDE 16

Woronichinia

Toxin – anatoxin, microcystin

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GENUS

ANABAENA ENTOPHYSALIS PULVINULARIA ANABAENOPSIS EUCAPSIS PSEUDANABAENA APHANIZOMENON FISCHERELLA RAPHIDIOPSIS APHANOCAPSA GLOEOCAPSA RHABDODERMA APHANOTHECE GLOEOTHECE RHABDOGLOEA ARTHROSPIRA GLOEOTRICHIA RIVULARIA AULOSIRA GOMPHOSPHAERIA ROMERIA BORZIA HAPALOSIPHON SCHIZOTHRIX CALOTHRIX HOMEOTHRIX SCYTONEMA CAMPTYLONEMOPSIS LEMMERMANNIELLA SNOWELLA CAPSOSIRA LYNGBYA SPHAEROZYGA CHAMAESIPHON MASTIGOCLADUS SPIRULINA CHROOCOCCUS MERISMOPEDIA STICHOSIPHON CHROOMONAS MICROCHAETE STIGONEMA CRINALIUM MICROCOLEUS SYNECHOCOCCUS COELOSPHAERIUM MICROCYSTIS SYNECHOCYSTIS COLEODESMIUM MICROCYSTIS culture TOLYPOTHRIX CYANOBIUM NODULARIA TRICHODESMIUM CYANOTHECE NOSTOC TRICHORMUS CYLINDROSPERMOPSIS OSCILLATORIA WOLLEA CYLINDROSPERMUM PLECTONEMA WORONICHINIA DACTYLOCOCCOPSIS PLEUROCAPSA DERMOCARPA PHORMIDIUM DICHOTHRIX PLECTONEMA

http://cfb.unh.edu/phycokey/Choices/Cyan

  • bacteria/cyano_1page/cyano_key.html
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SLIDE 18

Ecologically – cyanobacteria present carbon bottleneck Large / colonial – difficult to ingest by zooplankton (large plankters starve) Toxins have negative effects on zooplankton (although some not affected)

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SLIDE 19

1000 yrs ago General Zhu Ge‐Ling reported mortality in troops that drank water from a river in southern China that was green 1878 Australian lakes – livestock deaths 1980’s – livestock wildlife deaths in N. Idaho 1993 Idaho – cattle deaths at Cascade 1996 Brazil 52 humans in dialysis unit with contaminated water 2013 New Mexico – 100 Elk – exposure via drinking trough 2014 Toledo, OH drinking water intake shutdown 2017 Lakeview, OR cattle deaths 2018 Salem, OR cyanotoxins in water

CY CYANOBA ANOBACTERIA – TERIA – TOXINS INS history

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SLIDE 20
  • Endotoxins
  • Cytotoxins
  • Hepatotoxins
  • Neurotoxins

CY CYANOBA ANOBACTERIA – TERIA – TOXINS INS

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SLIDE 21
  • Endotoxins – Lipopolysaccharides (LPS)

‐ assoc. with outer membrane

CY CYANOBA ANOBACTERIA – TERIA – TOXINS INS

http://www.mncenter.org/issues/water http://www.mncenter.org/issues/water http://www.mncenter.org/issues/water

‐ skin rashes ‐ dermatoxins

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SLIDE 22
  • Cytotoxins – toxic to cells (necrosis)

CY CYANOBA ANOBACTERIA – TERIA – TOXINS INS

‐ breakdown of cell membrane

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SLIDE 23
  • Hepatotoxin – liver (hemorrhaging)

CY CYANOBA ANOBACTERIA – TERIA – TOXINS INS

‐ breakdown of cell membrane ‐ no antidote

http://www.bubblews.com/news/529637‐liver‐lover
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SLIDE 24

Necrosis in liver cells

Hemorrhage Necrosis and vacuolation

Theo Dreher and Robert J. Bildfell

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SLIDE 25
  • Neurotoxins – central nervous system

CY CYANOBA ANOBACTERIA – TERIA – TOXINS INS

‐ Affect 4 major components

‐ ion channels, acetylcholine receptors, synaptic vesicle peptides, and acetylcholine esterase

http://painprotherapeutics.com/conditions/neurological‐pain/

‐ Respiratory paralysis (rapid)

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SLIDE 26

Chemical structure of cyanotoxins (modified from Chorus 1999, USEPA 2019) Structure Cyanotoxin Primary target organ in mammals Cyanobacteria genera

Cyclic peptides

Microcystins

Liver

Microcystis, Anabaena, Planktothrix (Oscillatoria), Nostoc, Hapalosiphon, Anabaenopsis

Nodularins

Liver

Nodularia

Alkaloids

Anatoxin‐a

Central Nervous System Nerve synapse

Anabaena, Planktothrix (Oscillatoria), Aphanizomenon

Anatoxin‐a(S)

Nerve synapse

Anabaena

Cylindrospermopsins

Liver / kidney / lymphoid tissue

Cylindrospermopsis, Aphanizomenon, Umezakia

Lyngbyatoxin‐a

Skin, gastro‐intestinal tract

Lyngbya

Saxitoxin

Nerve synapse

Anabaena, Aphanizomenon, Lyngbya, Cylindrospermopsis

Lipopolysaccharides (LPS)

Potential irritant; affects any exposed tissue

All

Polyketides

Aplysiatoxins

Skin

Lyngbya, Schizothrix, Planktothrix (Oscillatoria)

Amino Acid

BMAA

Nervous System

All

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SLIDE 27

1/17/2019 Note – on previous slide – those toxins and species highlighted in yellow have been found in Idaho

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SLIDE 28

HUMAN HEAL HUMAN HEALTH EFFECT TH EFFECTS

  • Rashes
  • Hay fever‐like reactions
  • Flu‐like symptoms / nausea
  • Gastrointestinal upset (vomiting, diarrhea)
  • Death
  • Chronic exposure –

cancer rates, ALS etc.

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SLIDE 29

HUMAN HEAL HUMAN HEALTH EFFECT TH EFFECTS

  • Need to be careful about cause and effect
  • BMAA – beta‐Methylamino‐L‐alanine
  • Research suggests linkage to

Amyotrophic Lateral Sclerosis (ALS), Parkinsonism Dementia Complex (PDC)

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SLIDE 30

HUMAN HEAL HUMAN HEALTH EFFECT TH EFFECTS

Torbick et al. 2017. Assessing Cyanobacterial Harmful Algal Blooms as

Risk Factors for Amyotrophic Lateral Sclerosis. Neurotox Res (2018) 33:199–212

Caller, et al. 2012. Spatial clustering of Amyotrophic lateral sclerosis and the potential role of BMAA. Amyotrophic Lateral Sclerosis 13:25–32. Caller, et al. 2009. A cluster of Amyotrophic lateral sclerosis in New

Hampshire: A possible role for toxic cyanobacteria blooms. Amyotrophic Lateral Sclerosis 10:101–08.

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HUMAN HEAL HUMAN HEALTH EFFECT TH EFFECTS

Chernoff et al. 2017. A critical review of the postulated role of the

nonessential amino acid, β‐N‐methylamino‐L‐alanine, in neurodegenerative disease in humans. Journal of Toxicology and Environmental Health, Part B, DOI: 10.1080/10937404.2017.1297592

‐ call attention to ‘issues’ in previous studies ‐ mainly cautionary about cause / effect, not enough data to conclusively establish linkages

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SLIDE 32

HUMAN HEAL HUMAN HEALTH EFFECT TH EFFECTS

Many confounding factors obscure direct link between cyanotoxins and human illness (esp. at chronic level) Most incidences are retrospective analyses Potential for serious health consequences

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SLIDE 33

CONDITIONS THA CONDITIONS THAT PR PRODUCE BL ODUCE BLOOMS OOMS

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SLIDE 34

CONDITIONS THA CONDITIONS THAT PR PRODUCE BL ODUCE BLOOMS OOMS

  • Some indication of increase of incidence
  • Warm stagnant water
  • Nutrient imbalances
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SLIDE 35

Trophic state (continuum)

Oligo‐ Meso‐ Eutrophic

http://fitpacking.com/images/CLNP/CraterLakeAerial.jpg http://fitpacking.com/images/CLNP/CraterLakeAerial.jpg http://fitpacking.com/images/CLNP/CraterLakeAerial.jpg
  • F. Wilhelm
  • F. Wilhelm
  • F. Wilhelm
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SLIDE 36
  • presence of excess nutrients that

stimulate aquatic plant growth (Schindler et al. 2008)

Eutrophication

Coeur d’Alene Tribe

https://www.idahoecosystems.org/cda https://www.idahoecosystems.org/cda https://www.idahoecosystems.org/cda
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Natural trajectory of lakes

  • Oligotrophy to eutrophy

“Natural eutrophication” Tens of thousands of years…

http://bjornfree.com/galleries.html http://www.fingerlakes.org/uploads/pages/pdf/52.pdf

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SLIDE 38
  • accelerated natural process via human

activities

  • 10’s of years
  • Changes noticeable in human lifetime

Cultural eutrophication

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SLIDE 39

Most concerned about:

Nitrogen and Phosphorus

N:P

7:1 = balanced

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SLIDE 40
  • Theoretically

N:P > 7 = P-limited - OK

N:P ratio

N P :

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SLIDE 41
  • Theoretically

N:P > 7 = P-limited - OK N:P < 7 = N-limited - problems

N P :

N:P ratio

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SLIDE 42 T.Harris
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SLIDE 43
  • Favors cyanobacteria
  • Ability to fix N from atmosphere
  • Can overcome N-limitation

Low N:P ratio

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SLIDE 44
  • In reality, cyanobacteria blooms and

toxins occur when N:P is 75:1 or less

N:P ratio

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TN:TP

100 200 300 400 500 600 1100 1200

Total microcystin (µg/L)

50 100 150 200 500 600

Zurawell (unpublished) Ghadouani (unpublished) Graham et al. 2004 U.S. Lakes Survey 2007 Wilson (unpublished) Graham et al. 2006 Johnston & Jacoby 2003 Graham & Jones 2009 (W. CDN) n=40 (AUS) n=48 (Midwest USA) n=791 (USA) n=1253 (SE USA) n=702 (Midwest USA) n=254 (WA USA) n=59 (Midwest USA) n=1402 N=4549

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Need dual approach

i.

Reduce anthropogenic load

ii.

In‐lake management drop out P

  • r add N
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Add N – a nutrient

‐ considered a pollutant under CWA ‐ consider only for systems that are firmly in eutrophic state

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T N :T P

1 0 0 2 0 0 3 0 0 4 0 0 5 0 0

Cyano Biovolume (mm3/L)

2 .0 e + 1 1 4 .0 e + 1 1 6 .0 e + 1 1 8 .0 e + 1 1 1 .0 e + 1 2 1 .2 e + 1 2

r2 = 0 .9 9

Graham et al. 2004

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SLIDE 49

Mesocosms

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SLIDE 50
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J J A S O

TN:TP

100 200 300 400 500 600

Lake Enclosures

+N +N

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J A S

% Biovolume

20 40 60 80 100

Other Crypto Dino Chryso Diatom Green Cyano Toxic

LAKE PHYTOPLANKTON

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SLIDE 53

J A S

% Biovolume

20 40 60 80 100

Other Crypto Dino Chryso Diatom Green Cyano Toxic

MESOCOSM PHYTOPLANKTON

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SLIDE 54

Total nitrogen (mg/L)

1 2 3 4 5 6 7

Secchi depth (m)

2.0 2.5 3.0 3.5 4.0

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SLIDE 55

Lake Meso.

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J J A S O

TN:TP

100 200 300 400 500 600

Lake Enclosures

MICROCYSTIN DYNAMICS

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SLIDE 57

J J A S O

TN:TP

100 200 300 400 500 600

Microcystin (µg/L)

1 2 3 4 5

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IN-LAKE ADDITIONS OF N ARE IN-LAKE ADDITIONS OF N ARE SUCCESSFUL SUCCESSFUL

  • Dworshak Reservoir, ID
  • Kootenay Lake, BC
  • Various other BC lakes, rivers
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CY CYANOBA ANOBACTERIA / TO TERIA / TOXINS IN L XINS IN LONG-RANGE NG-RANGE TRANSPORT TRANSPORT, AND IN IRRIG , AND IN IRRIGATION W TION WATERS TERS

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SLIDE 60

Toxins measured 173 miles downstream

Graham et al. 2012

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SLIDE 61

(Preece et al., 2015a, 2015b)

Pacific blue mussels (Mytilus trossulus) exposed to freshwater discharges from lakes with CyanoHABs were found to contain toxins.

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SLIDE 62

Milwaukee Journal sentinel

(Lee et al. 2017)

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SP SPATIAL AND VERTIC IAL AND VERTICAL DISTRIBUTION L DISTRIBUTION OF CY OF CYANOBA ANOBACTERIA TERIA

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SLIDE 64
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SLIDE 65

Best practices for toxin monitoring

Surface scums CAN serve as indicators of toxic blooms (BUT NOT ALWAYS!)

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SLIDE 66

Microcystin concentration (ng/ml)

20 40 60 80 100 120

Secchi depth (m)

1 2 3 4

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SLIDE 67

What is depth distribution of blooms and toxins?

? ? ? ? ? ?

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2017 toxin results

µg/L

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2018 toxin results

µg/L

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SLIDE 70

Toxin concentrations across surface (2018)

Google Earth

MS WC BY UWC UBF BF

‐Even distributions within 0.5 µg/L ‐Highest concentration of 2.0 µg/L

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SLIDE 71

SP SPATIAL AND VERTIC IAL AND VERTICAL DISTRIBUTION L DISTRIBUTION OF CY OF CYANOBA ANOBACTERIA TERIA

Toxins occur at depth Scums good indicator of toxins (but not always) Scums are highly mobile Err on side of caution – sample scum

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SLIDE 72

Questions?

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