Diversity of marine

Images de @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

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

-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 (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)

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

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, and haptophytes ()

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 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

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 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 () Phylum

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) - = 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

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 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 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 « »

• 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 • mbs Eustigmatophyceae • 2 unequal flagella Phaeophyceae • Mastigonems « » ? Schizocladiophyceae Aurearenophyceaea Xanthophyceae Raphidophyceae Pinguiophyceae

Dichtyochophyceae

Pelagophyceae

Parmales - Bolidophyceae Bacillarriophyceae - Diatomophyceaee

Ochrophyta = (~16 classes – golden-) Silicoflagellates –

• 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,

Class described in 1995

Bolidophyceae ()

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 Protista: The Dazzling World of Living Cells List of Chapters

• Chapter 1 INTRODUCTION • Chapter 2 Chapter 16 Synurophytes • Chapter 3 Diplomonads Chapter 17 Diatoms Chapter 18 Brown algae • Chapter 4 Parabasilids Chapter 19 • 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 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 ) 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