Diversity of marine phytoplankton
Images de Plankton@net
Nathalie Simon January 2012 – UE EPHYBIO – Master 2 Phytoplankton : « wandering plants » mg/m3 0.1
1% of Chl 0.5 on earth 10
45% of Net Primary Production Ch a in Oceans Biological pump
Enrichment in inorganic C
Ci enrichment maintains excess C02 in oceans compared to atmosphere (Ocean : 300 ppm more CO2) …plancton Micro- Méso- (20-200 µm) (200µm-2mm)
Qqs mm Nano- (2-20 µm)
Pico- (0,2-2 µm) 0,4 µm
Finlay, 2002
Cyanobacteria Cyanobacteria
-Unicellular, trichoms, filaments -Bacterial Cellular Envelopp
PE I -Thylacoïds concentric, Chl a, carotenes, APC PC phycobilisomes (except for few genera PE II such as Prochlorococcus) -Genetic material: circular DNA, no histones
-Possibility for N2 fixation (hétérocystes) -Gaz Vacuoles (plankton) Synechocystis glycogène
granule de cyanophycine
carboxysome
ribosome
Mb externe 100 nm Peptidoglucane Liberton et al., 2006 Mb plasmique
Cyanobacteria : gram- Bacteria Marine planktonic cyanobacteria: ~14 genera? Trichodesmium -Trichomes organised in filaments
-Blooms (tropics)
-atm N2 Fixation
Richelia intracellularis ©LOB/K. Leblanc -Trichomes with heterocysts(Fixation N2 atm.)
- Symbiosis with diatoms (Guinardia, Hemiaulus,…)
©LOB/K. Leblanc (Photo by Dave Caron, Woods Hole Oceanographic Institution) Synechococcus Prochlorococcus « Crocosphaera »
Unicellular
Several genetic Several genetic Low genetic diversity clades clades
Antenna with Antenna with Antenna with Divinyl Chla/b phycobilisomes phycobilisomes
No N2 fixation No N2 fixation N2 Fixation 2 functionnal groups
1. Non diazotroph picocyanobacteria : major contribution to primary production in oligotrophic ocean (ex. adaptations : reduced size)
2. Filamentous diazotrophs : More than ½ of N import in tropics.
Primitive organisms with characters similar to those of PS Cyanobacteria p (-2,7 Billion years) are at the origin of atmospheric oxygenation (-2,3 Billion years).
2 functionnal groups
1. Non diazotroph picocyanobacteria : major contribution to primary production in oligotrophic ocean (ex. adaptations : reduced size)
2. Filamentous diazotrophs : More than ½ of N import in tropics.
Primitive organisms with characters similar to those of PS Cyanobacteria p (-2,7 Ma y) are at the origin of atmospheric oxygenation (-2,3 Ma ans), and are at the origin of all plastids. Plastids form a Synechococcus Prochlorococcus monophyletic group Phormidium Prochlorothrix Leptolyngbya Chamaesiphon
Nostoc, Calothrix, Scytonema, Cyano- Anabaena, Cylindrospermum Bacteria Oscillatoria, Trichodesmium, + Microcoleus, Arthrospira, Lyngbya Plastids Gloeothece, Gloeocapsa, Synechocystis Microcystis, Pleurocapsa, Prochloron Plastids Pseudanabaena Limnothrix
Unicellulars thermophiles
Strains phylogenetically close to Gloeobacter rDNA 16S Gloeobacter Turner (1997, 1999) Primary endosymbiosis and eukaryotic green (and red) algae
850-540 MY ago Neoproterozoic
Red algae
900-1200 MY ago Proterozoic : Primary Glaucophytes endosymbiosis Marine and freshwater
Land,fresh water Green algae
Plastids Starch in plastid Pigments : Chl a, b, néoxanthine
Flagella (0), (1), 2, 4, 2n Stellate structure
Cell wall Often with cellulosis Scales, theca or continuous Green algae in modern marine phytoplankton
thic Few genera (Dunaliella, Chlorella, Tetraselmis)
Some 10s genera Ostreococcus, Micromonas, … 140 described species Chlorophyceae Chlamydomonas, Dunaliella, …
- Cell wall or naked - Often 2 flagelles - Essentially salt marshes Trebouxiophyceae Chlorella, Nannochloris, Picochlorum, …
- Cell wall - No flagella (coccoids) Chlorodendrophyceae Tetraselmis
- Theca - 4 flagella « Prasinophytes »
• No unique derived character • Continuous cell wall, scales or naked • 8 clades (classes or classes to be described)
Scales « roues de Other scale bicyclettes » types (Mamiellophyceae) Example of scales on Pyramimonas obovata
Outer flagellar scale
Flagellar hair
Inner flagella Inner Intermediate Outer body scale body body scale scale scale
Lee (2005) Common coastal Pyramymonadales
Halosphaera Pterosperma
Walled cysts = phycomata Similar to microfossils such as Tasmanites and Cymatiosphaera reported from Precambrian Mamiellophyceae Widespread in marine picoplankton
Micromonas Ostreococcus
2 µm
0,5 µm Prasinophytes
Chlorarachniophyceae (« green spider web »), ~10 marine species
Lund & Lund (1995) Paulinella chromatophora
Cliché Web
Chlorarachnion reptans Geitler (1930) benthic or Bigelowiella picoplanctonic Diapositive de B. de Reviers, modifiée Envelopp 4 membranes
Thylacoïds by 3 (lamelles)
Nucleomorph
Chl. a + b
Chrysolaminarine (glucane b 1,3)
Mitochondrie with tubilar cristae
Lotharella “amoebiformis” strain Hajime Amoeboid cells
Secondary endosymbiosis 1200 MY?
Primary endosymbiosis 900-1200 MY? Diatoms, dinoflagellates and haptophytes (coccolithophores)
3 major groups of the micro- and nano-phytoplankton The fossil record 150 Diatoms species
100
Pangearifting Coccolithophorids
species Pannotiarifting
500 Dinoflagellates “species” cysts of dinoflagellate Ancestors? Acritarchs 50 Prasinophyte cysts Prasinophyte cysts “genera” +200m
Sea level 0 -100m Calcite seas Aragonite seas Calcite seas Intermittently anoxic deep ocean Deep oxic ocean After Katz et al. 2006 Paleozoic Tr J K Ceno 500 400 300 200 100 0 My B.P. Diapositive : W. Kooistra Dinoflagellates Alveolata, Dinophyta Dinophyceae
Important part of net primary production in the oceans
40% of marine phytoplankton species described
Nano - Microplankton
5000 species (2000 planktonic photosynthetic) Alveolata, Dinophyta, Dinophyceae
Alveoli under -2 flagella (T, L) plasmalemma - mitose particulière (fuseau externe)Peculiar mitosis Cell wall Alveoli under plasmalema, with/without cellulosis plates : naked / armored dinoflagellates
Alexandrium tamarense
Karenia brevis
Dinophysis acuta
From Lee (1989) and plankton@net
Epitheca Epicone
D G
Hypotheca, hypocone
Vue ventrale Armés / non armés
MO MO MO MO
MO
SEM
MO MO
SEM SEM SEM SEM Dinoconts Flagella inserted ventraly, in silts
Transverse Fl. (in cingulum)
Longitudinal Fl. (in sulcus)
Karenia brevis
Peridinium cinctum
Dorsal vue Ventral vue Desmoconts Modified from Lee, 1989 Ultrastructure
Nucleus (condensed chromosomes - Histones very peculiar - ~100 x more DNA than other euks)
Phycologia, mai 2004 Le dinokaryon, un noyau très particulier
Interphase Début division
Ségrégation des chromosomes (avec mise en place d’un canal cytoplasmique)
Division du noyau
B : Corps basaux, K : kinétochores, C : Chromosomes, NM : membrane nucléaire, Mt : Microtubules Ultrastructure
Trichocyst Chloroplasts •Most frequently •Envelop with 3 mbs, thylacoïds by 3 •Chl a, c, peridinin •Variations •Green, red plastids…
Nucleus (condensed chromosomes - Histones very peculiar - ~100 x more DNA than other euks)
Phycologia, mai 2004
Main storage: starch Gould et al., 2008 RCC1488 : Lepidodinium chlorophorum (isolée par I. Probert en Manche)
Photos de Chantal Billard Lepidodinium chlorophorum
Prasinophyceae : Pyramimonas Pyramimonas
SEM of the flagellated prasinophyte Pyramimonas gelidicola Image: Sandy Melloy Moestrup et Walne J. Cell Sci. 36, 437-459 0979) Ultrastructure
Trichocyst Chloroplasts •Most frequently •Envelop with 3 mbs, thylacoïds by 3 •Chl a, c, peridinin •Variations •Green, red plastids…
Nucleus (condensed chromosomes - Histones very peculiar - ~100 x more DNA than other euks)
Phycologia, mai 2004
Main storage: starch Projectiles (cnidocysts) Phototaxis, eyespots and ocellus
Mitochondria
Lens
Pigment cup
Canal Nematodinium armatum
« retinoid »=Fibrils (light reception) Bioluminescence
The Dinophyceae are the main contributors to marine bioluminescence, emitting a bluish- green (maximum wavelength at 474 nm) flash of light of 0.1-second duration when the cells are stimulated.
Possible structure of dinoflagellates luciferin Picture : Tara Ocean
Oxydized + 02 luciferin + Light Luciferase Major orders
Noctilucales: Highly mobile ventral tentacle
Gymnodiniales (+ Suessiales): athecate
Prorocentrales : 2 halves, lack cingulum
Dynophysiales : 2 halves
Gonyaulacales (+ Peridiniales) : 5 series thecal plates in alveoli Gomez (2012) Adaptation to planktonic life
• Colonies, cell wall spines and • Ethology : nyctemeral migrations extensions
Profil de Chl a durant un bloom de dinoflagellés (d ’après Eppley et al. 1968)
Phagotrophie Noctiluca
Polykrikos kofoides
Lee 2007 Nutrition par un « palium »
Un long filament Un pseudopode … et entoure la proie « attache » la proie descend le long qui est ensuite du filament digérée
Protoperidinium conicum Lee 2007 Myzocytose
Gymnodinium Pédoncule d’une Amphidinium fungiforme ingère le zoospore de cryophilum attaché à protoplasme de Pfiesteria pisciicida sa proie. Dunaliella salina (D) grâce à son pédoncule (P) Lee 2007 Haptophytes incl. coccolithophores
- 10 % of described marine phytoplankton spcecies (380 esp.) - Major role in biogeochemical cycles (C, du S) - Nanoplankton (picoplankton) Haptophytes incl. coccolithophores
• Synapomorphic character: haptonema
• Diversity - 400 - 500 species -nano- and picoplankton Haptonema •Variable size • 3 concentric membranes, 7 microtubules • mouvement and prey capture
Chrysochromulina
Lee (2008) Organic scales with/without calcification
Emiliania huxleyi
Chrysochromulina Coccolithus Hymenomonas http://microscope.mbl.edu/baypaul/microscope/general /page_01.htm Organic scales
•Proximal face : radially organised, sectors
•Distal face : variable, may include projections Phaeocystis
Cosmopolitan Harmful blooms (North Sea)
Références : Plankton@net, EOL, Lee (2008) 2 µm 0,2 µm
2 µm
Zingone et al. 2011) – Phaeocystis antarctica Coccoliths
Organic scales can 1/ Heterococcoliths provide a matrix for calcification Radial Arrangement Intact Coccolith of calcite cristals in vacuoles
2/ Holococcoliths
Extracellular Scale « matrix » precipitation
Dissolved Coccolith Emiliania huxleyi
John Green http://www.noc.soton.ac.uk/soes/staff/tt/eh/
True colour satellite image of a high reflectance Emiliania huxleyi bloom south of Plymouth, UK on the 30 July 1999..
Image: Remote Sensing Data Analysis Service (RSDAS) www.npm.ac.uk/rsdas/ of the Plymouth Marine Laboratory (PML) Diploid/ Haploid Emiliania huxleyi
2n n
Organic scales Coccoliths
Calciopagus rigidus (Mediterranée) Plankton@net Acanthoica quattrospina Papposphaera lepida Image: Remote Sensing Data Analysis Service (RSDAS) www.npm.ac.uk/rsdas/ of the Plymouth Marine Laboratory (PML) Other cytological and ultrastructural characters
2 flagelles égaux lisses (Prymnesiophyceae), inégaux chez les Pavlovophyceae
(1) ou 2 plastes bruns jaunes Enveloppe à 4 membranes, thylacoïdes groupés par 3 Chl a, c, diadinoxanthine, fucoxanthine, 19 ’-hexonoyloxyfucoxanthine
Réserve principales : glucane beta1-3 ramifié en beta 1-6
Couverture Phycologia Mai 2003 Classification Coccoliths
Prymnesiophyceae
Pavolovophyceae Knob Scales
Vargas et al. 2007 Vargas et al. 2007 Eukaryotes consensus phylogeny SAR Plantae
Habrobia
Unikonts
Excavates
Bauldauf 2008 The fossil record 150 Diatoms species
100
Pangearifting Coccolithophorids
species Pannotiarifting
500 Dinoflagellates “species” cysts of dinoflagellate Ancestors? Acritarchs 50 Prasinophyte cysts Prasinophyte cysts “genera” +200m
Sea level 0 -100m Calcite seas Aragonite seas Calcite seas Intermittently anoxic deep ocean Deep oxic ocean After Katz et al. 2006 Paleozoic Tr J K Ceno 500 400 300 200 100 0 My B.P. Diapositive : W. Kooistra Diatoms Belong to Heterokonta (Stramenopiles) Phylum Ochrophyta
Lee (2008) 40 % Of net Primary production by phytoplankton
40% of described species within phytoplankton
50 % of exported C
Microplankton (nanoplankton) Chap 11 vidéo Generalities about diatoms
-Photosynthetic, unicellular (forming colonies) -Frustule = silicified cell wall -Brown plastids
-10 000 species (> 2000 marine planktonic -Ecologically diverse
-Fossils and geological formations “diatomite” “tripoli” ou “kieselguhr” Frustule Epitheca
Hypotheca
Epivalve
Cingular band
Source : wikipedia
Drawings from : W. Kooistra Le frustule Vues valvaires Vue cingulaire
Les processus : projections à parois silicifiées
Thalassiosira eccentrica Plankton@net
Ornementations Processus (projections de silice)
Pores Areolae Chloroplast : Envelop with 4 membranes Groups of 3 thylacoïdes, lamella, pyrénoïd(s) or not Pigments : Chl a, c, fucoxanthin + caroténoïds
Storage material: Chrysolaminarin polyphosphates Lipid droplets
Van den Hoek, 1995 Origin of diatoms plastids
2 complete genomes E I = Cyanobacteria
Moustafa et al. Science 2010 : Origin of diatoms EII= Red algea genes identified through phylogenomics (among genes identified as originating from green or red algae)
Plastid originates from a Iiary endosymbiosis with red algae A Iiary endosymbiosis with a green algae could have left traces??? Radial Centrics Corethron
Stephanopyxis
Coscinodiscus Diapositive : W. Kooistra Multi-polar Centrics
Odontella
Thalassiosira
Chaetoceros
Diapositive : W. Kooistra Araphid Pennates
Fragilaria
Synedra
Licmophora Asterionella
Diapositive : W. Kooistra Raphid Pennates Pseudo-nitzschia
Entomoneis
Campylodiscus Diapositive : W. Kooistra Radial centrics
Multi-polar centrics
Araphid pennates
Raphid pennates
SSU
0.01 Diapositive : W. Kooistra 0 Frustules fossiles T Presence of pennates with raphe 65
90 Presence of pennates without raphe
K Antarctic ODP-Leg 693 Gersonde and Harwood, 1990 Australia Nikolaev and Harwood, 1997 120 Radial centrics and few multipolar
145 Calyptosporium, (Korea) Harwood et al., in prep. J Radial centrics Pyxidicula, (Germany) Rothpletz, 1896 180 Radial centrics
207 Tr
De W. Kooistra modifiée Ancestral benthic life style
Planktonic diatoms appeared several times in evolution
Benthic epiphytic Few pennate planktonic diatoms
Mobile on substrate
0.01 Modified from : W. Kooistra Chaetoceros et al.
Chaetoceros
Eucampia
Adaptations to live in the plankton © Jan Rines Diapositive : W. Kooistra Thalassiosirales
Thalassiosira
Skeletonema
Adaptations to live in the plankton Diapositive : W. Kooistra Asterionellopsis Thalassionema
Asterionellopsis
Asterionella
Thalassionema Asterionella
Pseudo-nitzschia and Fragilariopsis
Diapositive : W. Kooistra Trades-off : selection /adaptation Many opportinistic « bloomers »
Frustule
• Protection against predation • Flottability
Large vacuole
•Stocks of NO3-, PO42- •Allows to lower the amount available to competitors. Natural defenses of phytoplankton cells
Trades-off : protection / flottability
Smetacek, Nature Main functionnal groups : Silicifiers, calcifiers, + dinoflagellates
Diatomées
Dinoflagellés
Mandala de Margalef
Phytoplankton « Flagellates »
• Less studied, • Pico- and nanoplankton • Biomass and production important (outside bloom periods of dinos, diatoms, coccolithophores) Eukaryotes consensus phylogeny SAR Plantae
Habrobia
Unikonts
Excavates
Bauldauf 2008 Flagellates within phylum Ochrophyta Chrysophyceae • Chl a and c (incl. Synurales) • Golden brown Picophagus plastid Synchromophyceae • mbs Eustigmatophyceae • 2 unequal flagella Phaeophyceae • Mastigonems « Chrysomerophyceae » ? Schizocladiophyceae Phaeothamniophyceae Aurearenophyceaea Xanthophyceae Raphidophyceae Pinguiophyceae
Dichtyochophyceae
Pelagophyceae
Parmales - Bolidophyceae Bacillarriophyceae - Diatomophyceaee
Ochrophyta = (~16 classes – golden-brown algae) Silicoflagellates – Dictyochophyceae
• Genus Dictyocha : Constant in • Tentacules or « rhizopodes » on coastal water amoeboid cells • scales, spines or siliceous squeleton
Plankton*Net Data Provider at the Alfred Wegener Insitute for Polar and Marine Research
Lee (2008) Chap 12 - video Raphidophyceae
- 50 – 100 µm
- Numerous chloroplasts
-Mucocysts
-Verrucous Cells
- May be toxic
Ex : Chatonella, Heterosigma, Pelagophyceae
Class described in 1995
Bolidophyceae (parmales)
Class described in1999 Cryptophyta •Asymetric cells •2 flagella almost equal, lateral insersion stiff •1 or 2 plastids yellow, red or Poils greeen/blue •Vestibule with rows of ejectosomes
Cell wall = Pellicule 1 or several plaques on and under plasmalema (sandwich) Storage Env. à Starch in periplastidial compartment 4 mb PLASTID Plaques •Chl a, c2 de la •Phycoerythrin or phycocyanin in pellicule thylacoïds •Envelopp 4 membranes •Thylacoïds grouped by 2 Amidon •Nucléomorph Eukaryotes consensus phylogeny SAR Plantae
Habrobia
Unikonts
Excavates
Bauldauf 2008
)
3
- Surface Chl a (mgChl m Chl (mgChl a Surface
60°S 30°S 0° 30°N 60°N
Classes de taille (analyse des pigments marqueurs et de la couleur de l’océan)
Le Quéré et al. (2005) Global change Biology «Flagellates » in phytoplankton
• Belong to pico- and nanoplankton • Reservoir of unknown biodiversity • Morphological convergences : small size • Adaptations less studied than for microplankton Conclusions – present research fields
• Biodiversity description (incultivables, cryptic) • Mecanisms of evolution (macro- and microevolution) • Control of blooms, successions • Impact of abiotic environment (turbulence, nutrients, llight) and feed-backs • Biotic controls Adam Steiner, Le Jardin des sculptures, 1987, patio 45-56.
The Kingdom Protista: The Dazzling World of Living Cells List of Chapters
• Chapter 1 INTRODUCTION • Chapter 2 Choanoflagellates Chapter 16 Synurophytes • Chapter 3 Diplomonads Chapter 17 Diatoms Chapter 18 Brown algae • Chapter 4 Parabasilids Chapter 19 Oomycetes • Chapter 5 Cellular Slime Molds Chapter 20 Xanthophytes • Chapter 6 Acellular Slime Molds Chapter 21 Prymnesiophytes (Haptophytes) • Chapter 7 Amoebae: Rhizopods Chapter 22 Dinoflagellates • Chapter 8 Amoebae: Actinopods Chapter 23 Apicomplexans Chapter 24 Ciliates • Chapter 9 Chlorarachniophytes Chapter 25 Euglenids • Chapter 10 Cryptomonads Chapter 26 Kinetoplasts • Chapter 11 Raphidophytes Chapter 27 Glaucophytes • Chapter 12 Silicoflagellates Chapter 28 Red algae • Chapter 13 Pedinellids Chapter 29 Green Algae: Prasinophytes Chapter 30 Green Algae: Siphonous Groups • Chapter 14 Pelagomonads Chapter 31 Green Algae: Chlorophytes • Chapter 15 Chrysophytes Chapter 32 Green Algae: Charophytes Chapter 33 Protists and the Origin of GreenLand Plants Chapter 34 CREDITS -Localise the different groups in the consensus phylogenetic treee provided -Fill out the table with the main cytological, biochemical, ultrastructural characters of the different groups -Search ecologically important representatives of each of the groups in the litterature Molecular phylogenies : consensus tree Modern green alga are separated into 2 lineages
Mostly marine species Mostly freshwater species Modified from Lelliert et al. 2011 Few marine phytoplanktonic genera (Dunaliella, Chlorella, Tetraselmis)
« Prasinophytes » (Marine microalgae) 140 sp. Green algae in modern marine phytoplankton
Few marine phytoplanktonic genera (Dunaliella, Chlorella, Tetraselmis) Chlorodendrophyceae « Prasinophytes » (Marine microalgae) 140 sp.
Mamiellophyceae
CHLOROPHYTA : ~ 3500 species (marine and freshwater) CHLOROBIONTA
PHYLUM CHLOROPHYTA
PHYLUM STREPTOPHYTA
300 000 espèces 119 Becker et Marin 2009