Division Haptophyta = “Svepeflagellater”

Emiliania huxleyiPhoto: E. Paasche

ca 280 species and 75 genera

content

ecological significanceprincipal characteristics morphology and ultrastructurephylogenynutritiontaxonomycoccolith formationlife cyclesome members

Haptophyta - some members

Phaeocystis

Pleurochrysis

PrymnesiumCanter-Lund & Lund

Chrysotila

Hibberd

EmilianiaPaasche

Eikrem

Chrysochromulina

CalcidiscusCros & Fortuños

Ecological significance of Haptophyta

Descloitres, MODIS Rapid Response Team, NASA/GSFCTurner, Brazos River Authority

Paasche

Prymnesium parvum in Texas

Emiliania huxleyi / coccolithophorids

Dover cliffsOslofjord

Iceland

Effect on climate

Emiliania huxleyi, a cosmopolite, form blooms that influence global climate

DMSP = dimethylsulfoniopropionateDMS= dimethylsulfideacrylic acid

distribution and ecological significans

most are marine, present in all seas

mostly nanoplanktonic (2-20 µm)

important primary producers

highest diversity in tropical-subtropical open ocean

some may form extensive blooms

coccolithophorids influence biogeochemical processes

chalk (kritt) produced by coccolithophorids

Based on several genes and ultrastructure---- Lines suggested from environmental PCR Baldauf 2003. Science 300: 1703-6

Tree of Eukaryota

Chromalveolate hypothesis Cavalier-Smith

plastid in chromalveolates from a single endosymbioticevent

-> both host lineages and plastids share a common ancestor

Cavalier-Smith 2004. In: Hirt & Horner (eds).

Chromalveolate hypothesis

Harper et al. 2005: J. Syst. Evol. Microbiol. 55:487-496

analysis of six nuclear-encoded genes for cytoplasmic proteins in all major lineagesstrongly support heterokonts + alveolatesweakly support haptophytes + cryptophyteschromalveolates paraphyletic

number of coccolithophorid species over time

coccolithophorids in fossil records from ca 300-250 mill. years

(Carbon-Perm), but Haptophyta is probably > 600 mill. years

Several mass extinctions

Classification~75 genera, ~280 speciesUntil 1962 included in Chrysophyceae, ChromophytaHaptophyceae Christensen 1962 Prymnesiophyceae Hibberd 1976Haptophyta Hibberd ex. Edvardsen et Eikrem 2000Pavlovophyceae (Cavalier-Smith) Green et Medlin2000Prymnesiophyceae: 4 orders, Edvardsen et al. 2000Prymnesiophyceae: 6 orders, Jordan et al. 2004Prymnesiophyceae renamed to Coccolithophyceae, Silva et al. 2007.

General featuresTwo similar flagella with no tubular hairsHaptonemathe haptonema can coil or bend, but not beatit may adhere to substratum and be used in food handlingCells covered by organic scales Calcified scales (coccoliths) may be present

chloroplast

haptonema

flagella

scales

Throndsen

Ultrastructure

1-4, usually 2 chloroplasts4 plastid membranesthree thylacoids in lamellano girdle lamellachloroplast usually with pyrenoidGolgi (dictyosome) close to basal bodiesflagellar apparatus - a phylogenetic marker

Inouye 1997. Algae 12:247-61

Eikrem & Edvardsen 1999.Phycologia 38:149-55

Ultrastructure2 flagellahaptonema (H, 6-7 microtubuli)Golgi-apparatus (G)PER2-4 plastids3 lamella (L)chrysolaminaran (CHR)organic scales (SC)mucilage bodies (MB)4 membranes, 2ER+2CE Chrysochromulina

Flagellar root-system

R1, R2, R3 and R4 compound root in some species

chloroplasts, pigments and storage productgolden or yellow-brown chloroplasts with 4 membranestriple thylakoidsno girdle lamellapyrenoidPigments: kl. a, c1 og c2, c3,fucoxanthin, b-carotene, diatoxanthin, diadinoxanthin, 19’hexanoyloxyfucoxanthin,19’butanoyloxyfucoxanthinstorage product:chrysolaminaran

Function of haptonema “heftetråd”

to attachto handle food (in some Chrysochromulina)to avoid collisions

Food uptake

Prymnesiumcan ingestalgae and bacteria by phagotrophy

Toxin(s) paralyse and kill the prey

Prymnesium ingesting a green alga (Tillmann 1998)

Organic scalesEllipsoid organic scales with microfibrillarpattern

scales are species specific, but different life cycle stages may have different scale pattern

Scale pattern evident in TEM A Light micrograph of P. parvum

B Electron micrograph of scales

Photos: W. Eikrem

Morphology and ultrastructure in TEM

Chrysochromulinapringsheimii

Prymnesium parvum

Ultrastructure of coccolithophorid

coccoliths

vesicles from Golgi with coccolith

coccoid

Emiliania huxleyi

Heterococcolith formation in E. huxleyi

Formation of heterococcolith in E. huxleyi

frame of calcite crystals

Holococcoliths

Calyptrolithophorawith holococcoliths

holococcoliths consist of small, equally sized crystals

are formed extracellularly

Haplo-diploid heteromorphic lifecycle in Pleurochrysis carterae

Apistonema-stage, n

spores, 2n

Hymenomonas- stage, 2nmeiose

syngami

zooids, n

gamet, nzygot, 2n

Alternating heterococcolithophorid-holococcolithophorid life cycles

Knappertsbusch nhm

Coccolithus pelagicus Coccolithus pelagicus ssp. pelagicus HOL(= Crystallolithus hyalinus )

All holococcolithophorids are expected to be the haploid stage in the life cycle of a diploid heterococcolithophorid

nhm

Haptophyte phylogeny SSU rDNA

OLI16010OLI51080

OLI51076Crypthecodinium

OLI26047

Phaeocystis sp. 1

Phaeocystis antarcticaPhaeocystis pouchetii

Phaeocystis globosa

Phaeocystis sp. 2

OLI51004

Pavlova gyrans

Pavlova CCMP 1394Pavlova CCMP1416

Pavlova aff. salina

Fucus

}CLADE D

100/100

100/100

100/100

100/100

100/100

99/100

99/ 100

96/75

OLI51050OLI26041

Isochrysis galbanaPleurochrysis carteraeCCMP 300

Coccolithus pelagicusReticulosphaera japonensis

Emiliania huxleyi/Gephyrocapsa oceanicaCCMP 625

Pleurochrysis sp. CCMP 875Pleurochrysis elongata

Cruciplacolithus neohelis100/100

100/100

100/100

100/100

100/100

98/98

99/99

99/9993/74

65/89

87/57

76/6560/60

OLI16029

OLI16108OLI26017OLI51102

Chrysochromulina throndseniiChrysochromulina acantha

Chrysochromulina campanulifera

Chrysochromulina polylepisChrysochromulina kappa

Imantonia rotundaPrymnesium nemamethecum

Chrysochromulina hirta

Prymnesium calathiferumPrymnesium parvumPrymnesium patelliferum

OLI51059OLI51033, OLI51056

100/100

100/100

100/100

66/9879/98

79/8958/89 76/57

73/99

75/86

Chrysochromulina scutellum

99/67

97/100

98/97

100/100

2%

}CLADE E

-/60

66/-

Edvardsen et al. 2000. Phycologia 39:19-35.

ML-analysis

6 % divergence

Pavlovophyceae

Prymnesiophyceae

Prymnesiophyceae(=Coccolithophyceae)

Two smooth, more or less equal flagella inserted apicallyNo eyespot Cells usually covered by organic plate scales Mineralized scales (coccoliths) or spine scales may be present Haptonema may be conspicuous

Throndsen

Prymnesiophycean phylogeny SSU rDNA

OLI16010OLI51080

OLI51076Crypthecodinium

OLI26047

Phaeocystis sp. 1

Phaeocystis antarcticaPhaeocystis pouchetii

Phaeocystis globosa

Phaeocystis sp. 2

OLI51004

Pavlova gyrans

Pavlova CCMP 1394Pavlova CCMP1416

Pavlova aff. salina

Fucus

}CLADE A

CLADE C

}CLADE D

100/100

100/100

100/100

100/100

100/100

99/100

99/ 100

96/75

OLI51050OLI26041

Isochrysis galbanaPleurochrysis carteraeCCMP 300

Coccolithus pelagicus

Emiliania huxleyi/Gephyrocapsa oceanicaCCMP 625

Pleurochrysis sp. CCMP 875Pleurochrysis elongata

Cruciplacolithus neohelis

}100/100

100/100

100/100

100/100

100/100

98/98

99/99

99/9993/74

65/89

87/57

76/6560/60

OLI16029

OLI16108OLI26017OLI51102

Chrysochromulina throndseniiChrysochromulina acantha

Chrysochromulina campanulifera

Chrysochromulina polylepisChrysochromulina kappa

Imantonia rotundaPrymnesium nemamethecum

Chrysochromulina hirta

Prymnesium calathiferumPrymnesium parvumPrymnesium patelliferum

OLI51059OLI51033, OLI51056

}CLADE B1

}CLADE B2

100/100

100/100

100/100

66/9879/98

79/8958/89 76/57

73/99

75/86

Chrysochromulina scutellum

99/67

97/100

98/97

100/100

2%

}CLADE E

-/60

66/-

Based on Edvardsen et al. 2000. Phycologia 39:19-35.

ML-analysis

Reticulosphaera japonensis

Phaeocystales

Prymnesiales

Coccolithales

Isochrysidales

A. Phaeocystales

Swimming cells with two equalflagella and small plate scales

Short, stiff haptonema

Some produce filamentousstarlike structures

Some have a complex lifecycle that include a colonialstage with cells in a gelatinousmatrix

Phaeocystis pouchetii

Phaeocystis globosa

Zingone

Phaeocystis cordata

star of fibrils

Phaeocystis spp. life cycle

colony

Five stages are proposed for P. globosa:

1. Non-flagellated solitary cell, 2n

2. Non-flagllated cell in colony, 2n

3. Macroflagellates, 2n

4. Mesoflagellates, n

5. Microflagellates, n

Scum formation from Phaeocystis