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Algal Pigments As Biomarkers Linking Fish and Benthic Organisms with Type E Botulism

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Algal Pigments As Biomarkers Linking Fish and Benthic Organisms with Type E Botulism Algal pigments in benthic organisms and fish: development of biomarkers to trace food-web relationships Katherine T. Alben, Maxime Bridoux, Monika Sobiechowska Wadsworth Center, New York State Department of Health Dept. Environmental Health Sciences, SUNY-Albany National Water Quality Monitoring Conference May 9, 2006 San Jose, CA U at ALBANY From R. Ruffin, with permission Type E botulism: what are the food-web pathways? loon grebe gull Hypothesis: algal scud pigments goby yellow orange red can be used to trace food-web connections http://www.combat-fishing.com/lakepondbalance.htm#coldwaterlglake http://www.dnr.state.mn.us/exotics/aquaticanimals/roundgoby/index.html http://www.vancouverisland.com/021wildl&cons/wildlife/birds/cw/cw_herringgull.html http://www.admiraltyaudubon.org/ [email protected] U at ALBANY Algal carotenoids found in the food web diatoms & fucoxanthin C42H60O6 55 chrysophytes diatoxanthin C40H54O2 55 cryptophytes alloxanthin C40H52O2 55 chlorophytes lutein C40H56O2 (5) 55 5 cyanobacteria zeaxanthin C40H56O2 55 5 5 cantha- C40H52O2 55 β-crypto- C40H56O 55 echinenone C40H54O 555 euglenophytes neoxanthin C40H56O4 5 dinoflagellates peridinin C39H52O7 NF NF NF NF crustacean astaxanthin C40H52O4 55 5 5 metabolism U at ALBANY Method Development Standards – high resolution separations Quantitation – NIST, reference materials, MDLs Sample prep – microanalytical procedures, SPE, enzymatic hydrolysis Applications – Phytoplankton Gastropods Dreissenids Fish – round gobies, drum, perch, bass Standards - chlorophyll & carotenoids 1 - 5 mg amounts chlorophyll a SA ubiquitous astaxanthin SA crustacean chlorophyll b SA chlorophytes metabolism pheophorbide a WA chl a β-carotene SA ubiquitous degradation lycopene SA cryptophytes pheophytin a WA ubiquitous lutein CD chlorophytes β-cryptoxanthin CD cyanobacteria zeaxanthin CD cyanobacteria 6’R-α-carotene CN cryptophytes antheraxanthin CN chlorophytes, chrysophytes canthaxanthin CN cyanobacteria echinenone CN cyanobacteria fucoxanthin CN diatoms, chrysophytes neoxanthin CN chlorophytes, euglenophytes violaxanthin CN chlorophytes 2.5 mL @ 1.0 μg/mL chlorophyll c2 DHI cryptophytes alloxanthin DHI cryptophytes chrysophytes diadinoxanthin DHI diatoms, dinoflagellates diatoxanthin DHI chrysophytes, diatoms SA Sigma-Aldrich (Sigma, BioChemika) CD ChromaDex WA Wako (Japan) CN CaroteNature (Switzerland) DHI (Denmark) Spectrophotometric calibration of pigment stock solutions Conc (μg/mL) = Abs/(εb) ε (L/g-cm) extinction coefficient at λmax for designated solvent Spectrophotometer accuracy: NIST-traceable standard reference materials absorbance measurements, average error < tolerance limit 0.006 au-cm Grey-glass filters @440 nm @546 nm @635 nm G1 0.3 au-cm 0.0003 0.0000 0.0037 G3 0.5 au-cm - 0.0033 -0.0030 - 0.0029 G2 0.9 au-cm 0.0005 0.0009 0.0006 Perkin Elmer G2 @ 440.0 nm avg 0.9819 stdev 0.006 (0.6% ) 1.05 1.04 1.03 1.02 1.01 1.00 0.99 Abs (au) (au) Abs 0.98 0.97 0.96 0.95 0.94 0.93 4/1/2005 7/1/2005 9/30/2005 12/30/2005 4/1/2006 7/1/2006 9/30/2006 Time (mm/dd/yy) Preparation - mixed standards, 21 pigments final additions: large scale 300 μL HPLC buffer 50 μL IS per 4 mL small scale 45 μL HPLC buffer 7.5 μL IS per 600 μL 585 nm lights NH4acetate TBAA Analyses - Mixed Standards and Tissue Extracts Waters HPLC-PDA 625 pump controller (ternary) 717 autosampler 996 photodiode array detector 200 - 800 nm 474 fluorescence detector Empower data system Agilent-Thermoquest LC-MS 1100 pump system (binary) 1100 autosampler 1100 column heater 1100 single wavelength detector LCQ ion-trap mass spectrometer with ESI (electrospray) and APCI (atmospheric pressure-chemical ionization) sources Xcaliber data system U at ALBANY Identify Pigments - HPLC retention times high-resolution separations: 20 pigments canth Agilent 3 μm C18 25 cm λ 408 nm o 60 60 C diad allo IS echi pht HPLC solvent program anth diato mau fuco asta modified Wright & Jeffrey 30 neo lutein phb viola chl a (1991, 1997) α-caro b crypto β-caro chl c2 chl b lyco A 80:20 MeOH: 0.5 M NH4acetate:H2O 0.0 B 90:10 MeCN:H2O 10. 20. 30. C ethyl acetate Minutes Identify Pigments - HPLC retention times high-resolution separations: 21 pigments cantha echi Agilent 3 μm C8 25 cm o λ 408 nm 60 C 60 allo diato diad anth HPLC solvent program lut zea IS β crypto modified Van Heukelem viola pht mau asta chl a Thomas 2001 30 phb neo α-caro β-caro fuco A 70:30 MeOH: chl c2 chl b lyco 28 mM TBAA:H2O 0 BMeOH 10. 20. 30. Minutes Identify Pigments - PDA spectra 300 - 800 nm diatoms chlorophytes cryptophytes 449 fuco 441 471 viola 80 454 483 allo 7.62 8.10 8.96 40 417 20 40 20 0 0 0 120 448 diadino 448 lutein 455 482 β-caro mau 478 476 8.52 200 9.63 20.25 80 40 100 40 0 0 0 400 600 800 400 600 800 400 600 800 U at ALBANY Quantify pigments multilevel mixed standards - reproducibility, 3 mos lutein 1.5E+06 11% 1.0E+06 Area 5.0E+05 35% 0.0E+00 0.0 0.2 0.4 0.6 0.8 1.0 Concentration (μg/mL) U at ALBANY Reference culture: diatom UTCC 542 Fragilaria crotonensis μg/106 cells μg/106 cells chlorophyll a 1.60 fucoxanthin 1.05 0.31 - 5.3 chlorophyllide 1.66 diadinoxanthin 0.33 Roy et al pheophytin a 0.02 β-carotene 0.07 1996 St Lawr R 408 chl a 300 λ fuco 200 chlide diadino mau 100 IS 0 0 10 RT(minutes) 20 http://protist.i.hosei.ac.jp/PDB/Images/Heterokontophyta/Araphidineae/Fragilaria/Fragilaria.jpg U at ALBANY Reference culture: cryptophyte UTCC 344 Rhodomonas minuta μg/106 cells μg/106 cells chlorophyll a 0.349 alloxanthin 0.101 0.19 -0.28 chlorophyll c2 0.042 β-carotene 0.019 Roy et al pheophytin a 0.004 1996 St Lawr R λ 448 allo 1.60 1.20 0.80 au chl a chl c2 0.40 β caro IS pht 0.00 0 10 20 RT(minutes) http://huey.colorado.edu/LTER/images/pictures/lakes/plankton/rhodomonas/Rhodomonas_891204_T2D_8.0.html U at ALBANY Reference culture: filamentous chlorophyte UTCC 13 Cladophora glomerata (L.) Kutzing μg/g ww μg/g ww chlorophyll a 1079 lutein 100 chlorophyll b 721 violaxanthin 133 pheophytin a 12 β-carotene 91 λ 448 chl b 1.2 0.8 lutein au viola 0.4 chl a β caro IS 0.0 0 10 20 RT(minutes) http://vis-pc.plantbio.ohiou.edu/algaeimage/pages/Cladophora.html U at ALBANY Lake Ontario: Cladophora glomerata μg/g ww μg/g ww chlorophyll a 107.3 lutein 7.0 chlorophyll b 70.6 violaxanthin 5.7 pheophorbide a 15.7 β-carotene 4.1 pheophytin a 4.8 fucoxanthin 37.5 diatoms chlorophyllide 1.2 diadinoxanthin 2.0 600 λ 448 chl b 400 fuco mau 200 lutein chl a vio IS β caro 0 0 10 20 RT(minutes) U at ALBANY Epiphytic diatoms 3 μm Cocconeis pediculus on fiber of Cladophora glomerata Stevenson Stoermer 1982 100 μm U at ALBANY Lake Ontario gastropods 408 phb ester pyropht 400 λ pht(s) 200 phb phyllide(s) 1 cm pht a 0 400 λ 448 fuco μg/g ww pheophytin a 1.5 mau pyropheophytin 26.2 200 caro β-caro fucoxanthin 29.0 diatoms caro allo alloxanthin 4.4 β-carotene 11.2 0 10 20 RT(minutes) U at ALBANY Epiphytic diatoms → ingested diatoms ← Cocconeis pediculus in snail tissue ∴ ingested 3 μm Cocconeis pediculus on snail shell → 10 μm U at ALBANY Case study #1: conclusions Carotenoid biomarkers for diet epiphytic gastropods ~ grazers ~ epiphytic diatoms first trophic level ← primary productivity (diatoms) HO OAc 449 fucoxanthin O 20 O HO 0 C42H60O6 fucoxanthin on-going studies Analysis of other benthic organisms (oligochaetes, tubificids, diptera etc) - senescent phytoplankton Analysis of fish (and birds) that eat snails U at ALBANY Case study #2: quagga mussels & phytoplankton dreissenid invasion of Great Lakes: benthic filter feeders (~1 L/day/mussel) reduced chlorophyll a, phytoplankton biomass (MacIssac et al 1992; Horgan & Mills 1997; many others) U at ALBANY HPLC-photodiode array analysis 40 Group II Ontario mussels Group I 20 phb(s) allo λ 448 λ 442 0 max max Erie phb(s) Group I mau 80 mussels Group II 40 allo IS zea cyanobacteria Barbiero Tuchman 2000 λ 448 λ 442 0 max max 0 10 Minutes 20 U at ALBANY Algal biomarkers in mussel tissue 409.8 pyropheophorbide 40 degradation of chlorophylls 666.1 - digestion by mussels 20 0 453.6 482.9 alloxanthin 80 40 cryptophytes mau 0 452.4 479.3 zeaxanthin 40 cyanobacteria - Lake Erie 20 0 Barbiero Tuchman 2000 300 500 700 nm U at ALBANY Group I & II pigments: hydrophobic (late eluting) 40 Group II Ontario mussels Group I 20 phb(s) allo λ 448 λ 442 0 max max Erie phb(s) Group I mau 80 mussels Group II 40 allo IS zea λ 448 λ 442 0 max max 0 10 Minutes 20 U at ALBANY Group I cluster: identification 160 448.7 group I 447.5 fucoxanthin 25 standard 15 80 Library: fucoxanthin chromophore 5 mau 0 300 500 700 300 500 700 nm nm HO OAc O O HO pigment fingerprint of diatoms U at ALBANY Group I: carotenoid fatty-acid monoesters Xanthophyll pigments: 1 or more hydroxyl groups HO OAc Hydroxyl available to be esterified by fatty acids O O fucoxanthin HO esters typically have spectrum of parent carotenoid esterification chromophore (Carotenoid HO OAc Handbook, Britton, Liaaen- Jensen, Pfander) O O O O fatty acid monoester (eg C16 - palmitate) FAs saturated monounsaturated PUFAs C14:0, C16:0, C18:1n9 C18:3ω3, C18:2ω6, C20:5ω3 C18:0, C20:0 C20:4ω6, C22:6ω3 U at ALBANY Group II cluster: carotenoid fatty-acid diesters 441.4 470.7 441.4 470.7 15 group II 40 violaxanthin standard 10 Library mau 20 5 violaxanthin chromophore 0 0 800 400 600 400 nm nm 600 800 OH O O HO pigment fingerprint of chlorophytes O O O O O O violaxanthin diester (C16:0) (C16:0) U at ALBANY SEM: ingested diatoms, from mussel tissues pennate (Fragilaria) & centric centric 2 μm centric 5 µm 10 μm Credit:Monika Sobiechowska 2005 U at ALBANY Quantitation pigment Lake Ontario Lake Erie (μg/g ww) (μg/g ww) pyropheophorbide
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