Biogeochemistry (2007) 83:3–18 DOI 10.1007/s10533-007-9087-1

REVIEW PAPER

A taxonomic review of the genus Phaeocystis

Linda Medlin · Adriana Zingone

Received: 20 October 2005 / Accepted: 22 August 2006 / Published online: 15 March 2007 © Springer Science+Business Media B.V. 2007

Abstract Phaeocystis is recognized both as a multiple diVerent ITS copies, suggestive of cryptic nuisance and as an ecologically important phyto- species that are still able to hybridize. A molecu- plankton species. Its polymorphic life cycle with lar clock has been constructed that estimates the both colonial and Xagellated cells causes many divergence of the cold water colonial forms from taxonomic problems. Sequence variation among the warm-water colonial forms to be about 30 Ma 22 isolates representing a global distribution of and the divergence of P. antarctica and P. pouch- the genus has been compared using three molecu- etii to be about 15 Ma. A short description of the lar markers. The ribulose-1,5-bisphosphate car- colonial stage and the Xagellated stage for each boxylase/oxygenase (RUBISCO) spacer is too formally recognized species is provided. Morpho- conserved to resolve species. The most conserved logical information is also provided on a number 18S ribosomal deoxyribonucleic acid (rDNA) of undescribed species. These include the strain analysis suggests that an undescribed unicellular Ply 559, consisting of non-colonial cells with pecu- Phaeocystis sp. (isolate PLY559) is a sister taxon liar tubular extrusomes, a second non-colonial to the Mediterranean unicellular Phaeocystis species from the north western Mediterranean jahnii; this clade branched prior to the divergence Sea producing a lot of mucus, and a colonial spe- of all other Phaeocystis species, including the colo- cies with scale-less Xagellates found in Italian nial ones. The internal transcribed spacer (ITS) waters. In addition, three Xagellated morphotypes region shows suYcient variation that some spatial with scales diVerent from those of P. antarctica population structure can be recovered, at least in were reported in the literature from Antarctic P. antarctica. P. globosa and P. pouchetii have waters. The picture emerging from both molecu- lar and morphological data is that the number of species in the genus is still underestimated and that cryptic or pseudocryptic diversity requires a sound assessment in future research of this genus. L. Medlin (&) Based on all published observations, an emended Alfred Wegener Institute for Polar and Marine Research, Am Handelshafen 12, Bremerhaven, 27570, description of the genus is provided. Germany e-mail: [email protected] Keywords Molecular clock · Phaeocystis antarctica · P. cordata · P. globosa · A. Zingone Stazione Zoologica Anton Dohrn, Villa Comunale, P. jahnii · P. pouchetii · P. scrobiculata · 80121 Naples, Italy rDNA analysis

123 4 Biogeochemistry (2007) 83:3–18

Introduction of diVerent shaped organic scales. Some Xagel- lated cells also produce groups of Wlaments, which Phaeocystis Lagerheim is a cosmopolitan bloom- are extruded from the cell and assume a charac- forming alga that is often recognized both as a teristic pattern. nuisance alga and an ecologically important member The genus was erected by Lagerheim in 1893 to of the phytoplankton (Davidson 1985; Lancelot accommodate the colonial stage of an alga et al. 1987; Smith et al. 1991; Davidson and described originally as Tetraspora poucheti by Marchant 1992; Baumann et al. 1994; Schoemann Hariot in Pouchet (1892). Phaeocystis pouchetii et al. 2005; Veldhuis and Wassmann 2005). Its (its correct orthography) occurs in cold waters various life forms can make large-scale blooms and in its globular, lobed colonies, cells are that are often avoided by Wsh (Chang 1983) and arranged in packets of four (see Jahnke and appear detrimental to the growth and reproduc- Baumann 1987 for illustrations). Phaeocystis tion of shellWsh and macrozooplankton (Davidson globosa was described by ScherVel (1900) from and Marchant 1992) or are ichthyotoxic (Shen temperate waters and forms spherical colonies with et al. 2004). Massive areas of pollution are created cells arranged homogeneously within the colony when dissolved organic compounds released by (Jahnke and Baumann 1987), whereas older Phaeocystis during declining bloom conditions stages can assume distorted pear shapes (Bätje accumulate, foam and then wash onshore (Lancelot and Michaelis 1986). Early workers separated et al. 1987). Phaeocystis is a major contributor to P. pouchetii and P. globosa based on diVerent the global sulphur budget by releasing substantial distributions and colonial morphologies until quantities of dimethylsulWde propionate (DMSP) Kornmann (1955) doubted the diVerentiation (Keller et al. 1989; Baumann et al. 1993), which is between the two species. From his life-cycle studies, metabolized to dimethylsulWde (DMS) as the cells he considered that P. globosa cell types appeared are grazed or infected and lysed by viruses. It may to be juvenile forms of P. pouchetii. Since that play yet another important ecological role with its report, colony morphology has been judged an production of ultraviolet B (UV-B)-absorbing unreliable speciWc character. compounds (Marchant et al. 1991; Davidson and Sournia (1988) reviewed the diagnostic Marchant 1992). features of Phaeocystis, and discussed the reliability Phaeocystis has a polymorphic life cycle with of the nine valid species published since the last both colonial and Xagellated cells (Kornmann century. He discarded two species from the genus, 1955; Whipple et al. 2005). The colonial stage, P. fuscescens (Braun) De Toni and P. giraudyi with cells very loosely interconnected and (Derbès and Solier) Hamel, because they did not enclosed in a thin skin (Hamm et al. 1999), is Wt the genus and probably not even the class char- most easily recognized, although some species acteristics. The descriptions of four species, two may form mucilaginous colonies or do not seem from cold waters, P. antarctica Karsten and to have a colonial stage. Thousands of cells can P. brucei Mangin, and two from temperate waters, occur in a colony that may reach 2 cm in diameter P. amoeboidea Büttner and P. sphaeroidea Bütt- (Jahnke and Baumann 1987; Verity et al. 1988; ner, were all judged as very superWcial. The poor Rousseau et al. 1994; Davidson and Marchant illustrations and unlikely features, including one 1992). Colony sizes of 3 cm or more have been chloroplast per cell and no haptonema (Büttner reported in blooms from China (Shen et al. 2004). 1911), were probably the reasons why the two The diYculty in assigning a speciWc name to the temperate species have never been mentioned colonial stage has caused much taxonomic confu- again in the literature. For similar reasons the two sion. Flagellated cells have two parietal chlorop- Antarctic species were reported rarely and not lasts and two Xagella, which may be equal or studied again. As for the two most frequently unequal in length and heterodynamic. A short recorded species, P. pouchetii (Hariot in Pouchet) haptonema is present between the two Xagella, Lagerheim and P. globosa ScherVel, they had which may or may not have a swollen end. The been studied in more detail yet no element was Xagellated cells may be naked or have two layers available to keep them separate. Therefore Sournia

123 Biogeochemistry (2007) 83:3–18 5 suggested that the name P. pouchetii or, better, isolates previously termed P. globosa or pouchetii P. cf. pouchetii should have been used for the from these waters. Zingone et al. (1999) added colonial Phaeocystis species pending new infor- two more species to the genus, P. cordata and mation. The only other reliable species was Phae- P. jahnii, but these were basically unicellular spe- ocystis scrobiculata Moestrup, described with cies, although the latter species could make simple modern methods but known only from the Xagel- clusters of cells that could be termed colonial. In lated state (Moestrup 1979). Without convincing this review we summarize the molecular and mor- information on the diVerentiation between phological information available to date for Phae- P. pouchetii and P. globosa (see paragraph below), ocystis species and provide evidence that a high most marine ecologists until the mid 1990s fol- diversity is still hidden in the genus. lowed Sournia’s advice and reported Phaeocystis colonies as P. pouchetii (the older name) or as Phaeocystis sp. to avoid confusion. Molecular analysis Baumann and Jahnke (1986), Jahnke and Baumann (1986, 1987) and Jahnke (1989) regarded A global distribution of the prymnesiophyte this as over-simpliWcation. Their observations on genus Phaeocystis was compared using nuclear- colony shape maintenance in long term culture encoded 18S rDNA genes and two non-coding showed that both juvenile and older stages of regions, the ribosomal DNA internal transcribed P. globosa and P. pouchetii were distinct and these spacer 1 (ITS1) separating the 18S rDNA and data supported the recognition of the two entities 5.8S rDNA genes and the plastid ribulose-1,5-bis- as separate species. Also, detailed studies of the phosphate carboxylase/oxygenase (RUBISCO) temperature and light tolerances suggested sepa- spacer Xanked by short stretches of the adjacent ration at the species level. P. globosa was a tem- large and small subunits (rbcL and rbcS) (Lange perate species and P. pouchetii was a cold-water et al., 2002). The RUBISCO spacer regions were form. A third, unnamed colonial species from highly conserved and generally uninformative Antarctic waters was recognized by Baumann among all Phaeocystis strains (Lange et al. 2002). et al. (1993), which had a combination of features The 18S rDNA analysis suggests that an unde- of P. globosa and pouchetii, as suggested earlier scribed unicellular Phaeocystis sp. (isolate by Moestrup and Larsen (1992). The colonies PLY559) is a sister taxon to the occasionally colo- resembled those of P. globosa (Larsen and nial Mediterranean P. jahnii with which it forms a Moestrup 1989), whereas temperature tolerance clade that diverges at the same time from a clade was similar to that of P. pouchetii. Notably, strains with all other Phaeocystis species, including those from the Antarctic had diVerent pigment spectra forming typical colonies wrapped in a skin (Buma et al. 1991; Vaulot et al. 1994) and DNA (Fig. 1). In this latter clade, the unicellular P. cor- content (Vaulot et al. 1994). First indications that data diverges before the colonial ones, which can further undescribed species could exist were pro- be divided into a cold-water complex (P. pouch- vided by Pienaar (1991, 1996) who illustrated a etii from the Arctic and P. antarctica from the Phaeocystis Xagellate with cup-shaped scales from Antarctic) and a warm-water complex consisting South African waters suggesting it was a new spe- of P. globosa. Thus, all of the variation seen ear- cies but not publishing a formal description. lier using morphological and physiological criteria To resolve the species issue in Phaeocystis, a had a strong genetic basis and separation at the molecular analysis of various clones was begun species level was warranted for all colonial spe- (Lange 1997). Medlin et al. (1994) were the Wrst to cies originating from major climatic regions, i.e., propose that P. globosa and P. pouchetii were sep- the Arctic, the Antarctic and temperate/tropical arate species based on genetic evidence. They also regions. showed that colonial Phaeocystis from the Antarc- In contrast, ITS1 exhibited substantial inter- tic was genetically distinct from the other two spe- and intra-speciWc sequence divergence and cies. They resurrected the species P. antarctica showed more resolution among the strains described by Karsten (1905) for the colonial (Fig. 2). Markedly diVerent copies of the ITS1

123 6 Biogeochemistry (2007) 83:3–18

Fig. 1 Maximum-likeli- hood phylogeny (fastD- NAml) of 17 Phaeocystis species/strains and other prymnesiophytes inferred from 18S rDNA. The class Pavlovophyceae was used as outgroup. Bootstrap values are placed on the nodes that are identical from ML/NJ/MP analyses. The scale bar corresponds to two base changes per 100 nucleotides. Redrawn from Lange et al. (2002)

region were found in P. globosa even among graphic history of the dispersal of strains in Ant- cloned DNA from a single strain, suggesting that arctic coastal waters. We see that the Wrst it is a species complex composed of at least three divergence among the Antarctic clade is strain SK species. This observation was also supported by 22, which was isolated from the Antarctic circum- diVerent DNA content among diVerent clones of polar current (ACC). The second divergence is a Phaeocystis (Vaulot et al. 1994). Multiple copies strain from Prydz Bay (T4-2) and this is then fol- of the ITS1 were also found in a single strain of P. lowed by a nearly simultaneous divergence of the pouchetii, suggesting that this is also a species remaining strains. Among these divergences is a complex. These species complexes would appear cluster of strains from Prydz Bay (DE2, A1-3 and still to be able to interbreed with one another T9-1). The other divergence includes strain because multiple diVerent haplotypes from diVer- CCMP 1374 from the Ross Sea and two Phaeo- ent clades can be found within a single strain. cystis strains from the Weddell Sea (SK 20, SK Similar Wndings of multiple haplotypes being 23) (Fig. 3) and Wnally strain D4-5 from Prydz present in known hybrids of Xowering plant spe- Bay, which shares a last common ancestor with cies are quite common (Chase et al 2003) and it is the Weddell Sea strain SK 23, as the Wnal cluster known that in some hybrids of Xowering plants, to diverge among the Antarctic strains. Popula- the hybrid can loose one of the parental haplo- tions of P. antarctica within the continental types in as few as 12 generations (Bateman, pers. boundary water masses appear to be well-mixed com.) However, among nine P. antarctica strains, because currents move around the Antarctic con- only one type of ITS1 haplotype was found per tinent rather quickly and may eVectively act as a strain, although it was variable among the strains. barrier to signiWcant population structure. Strain Using the branching order in the ITS1 tree SK 22 isolated within the ACC, however, is (Fig. 3) we have attempted to trace the biogeo- clearly diVerent. An earlier hypothesis, proposed

123 Biogeochemistry (2007) 83:3–18 7

Fig. 2 Maximum-likeli- hood phylogeny of the ITS regions showing the multiple sequences from a single strain of P. globosa and P. pouchetii. Each diVerent sequence comes from a diVerent bacterial vector clone. All haplo- types from one strain of Phaeocystis are connected by the arrows. P. antarc- tica exhibited a single se- quence per strain and these are collapsed into a triangle. Redrawn from Lange et al. (2002)

from rDNA data (Medlin et al. 1994), that ances- ing event will then isolate the two polar popula- tral populations in the Antarctic gave rise to pres- tions. Evidence for this can be found in a study of ent day P. antarctica and P. pouchetii populations Antarctic surface-water temperatures since the appears to be supported by ITS1 analysis of the Cretaceous (Crame 1993, Fig. 4c). cold-water Phaeocystis strains. P. antarctica and If we follow the branching order in Fig. 1, we P. pouchetii, both polar, are more closely related hypothesize the following scenario: Phaeocystis to one another than either is to the cold and warm likely originated as a warm-water genus because temperate to tropical populations of present-day Wrst divergences in our tree are warm-water spe- P. globosa. This suggests that dispersal did not cies. Ancestral populations in the Antarctic were occur from present-day warm-water populations derived from ancestors of the present-day warm- into present-day cold-water populations but that water species, after being isolated in Antarctic gene Xow has occurred from pole to pole across waters. The opening of the Drake passage and the tropical oceans. Arctic P. pouchetii populations formation of the Antarctic circumpolar current thus probably arose by a dispersal event from the (ACC) are the most likely geological events that south to the north during colder climate periods could have isolated populations in the Antarctic that allowed populations to survive the crossing to separate them from warm-water ancestors. It of equatorial waters, as has been documented for can be inferred from Fig. 3 that presumed descen- other organisms (Crame 1993; Darling et al. 2000, dants of these warm-water ancestors were Wrst 2004; Montresor et al. 2003). A subsequent warm- entrained in the ACC because these are the Wrst

123 8 Biogeochemistry (2007) 83:3–18

Fig. 3 we can trace the dispersal of the clones from the ACC, although the bootstrap support for the branching order is weak to strong among the clades. The Wrst entrainment with a bootstrap support of 99% appears to be into Prydz Bay because strain T4–2 isolated from this bay is the Wrst divergence in our tree. These populations then established themselves in the Eastern Ant- arctic in Prydz Bay. Subsequent divergences in the tree indicate that populations were then entrained into the Ross Sea and almost simulta- neously they were entrained into the Weddell Sea (bootstrap support 54%). Both isolates from the Weddell Sea were the last to diverge before the populations were again entrained back into Prydz Bay from populations in the Weddell Sea because isolates from this bay are some of the last diver- gences in the tree (bootstrap 54%). The distribu- tion of these isolates in this fashion follows the predominant current patterns of surface waters in the Antarctic today. What we do not know is how diVerent the surface-water circulation was 30 Ma before the ACC was established. Other studies have also shown the eVect of mixing on the homogenization of the genetic structure of Antarctic populations. Krill species within the Antarctic continental water masses are very similar as documented by both mtDNA Fig. 3 (a) Locations of the strains of P. antarctica used in (Patarnello et al. unpubl.) and isozyme analysis Lange et al. (2002). The location of diVerent clades is indi- cated by the diVerent patterns in the large circles and cor- (Fevolden and Schneppenheim 1989). The mtDNA respond to those clades in (b). Prydz Bay locations in study also suggested that the formation of the E. Antarctica are slightly displaced for visual clarity. (b) ACC eVectively isolated krill species in Antarctic Maximum-likelihood tree inferred from ITS1 sequences water masses from those north of the ACC. from P. antarctica with P. pouchetii as outgroup. Bootstrap values are placed at the nodes from a maximum likelihood Calculation of the time of divergence between analysis (100 replicates) a neighbor-joining analysis species groups found either side of the ACC coin- (500 replicates) and a maximum parsimony analysis cided with the timing of the ACC, approximately (500 replicates). The scale bar corresponds to two changes 30 Ma. Thus, the molecular data is consistent with per 100 nucleotide positions. Redrawn from Lange et al. (2002). Map of Antarctica redrawn from Olbers et al. our hypothesized historical biogeographic recon- (1962) struction of the distribution of Phaeocystis based on the circulation patterns developed with the divergences. Some of these ancestral populations formation of the ACC. must have been transported northward and across the Equator shortly after the Drake passage opened because the P. pouchetii populations are Molecular clock sister to the P. antarctica populations. The ACC today encircles the Antarctic continent every A molecular clock has been constructed from our 1–2 years. Water is entrained from this current 18S rDNA tree and calibrated with fossil dates into the major gyres of the continental water masses from the haptophyte coccolithophorid species (Treshnikov 1964). Using the branching order in (Fig. 4). Our molecular clock calculations indicate

123 Biogeochemistry (2007) 83:3–18 9

Fucus Pavlova gyrans (a) Diacronema vlkianum Pavlova lutheri Pavlova sp. CCMP1416 Pavlova virescens Exanthemachrysis gayraliae Rebecca salina OLI 51059 CCMP 1204 Imantonia rotunda Imantonia sp. CCMP 1404 Chrysochromulina brevifilum Chrysochromulina hirta Chrysochromulina herdlensis Chrysochromulina chiton Chrysochromulina minor Chrysochromulina polylepis Platychrysis pigra Platychrysis simplex Prymnesium parvum Prymnesium tunis Prymnesium faveolatum Prymnesium calathiferum Chrysochromulina kappa Chrysochromulina spinifera Chrysochromulina parva Chrysochromulina rotalis Chrysochromulina throndsenii Chrysochromulina cf. ephippium OLI 16029 OLI 51102 OLI 26017 OLI 16108 Chrysochromulina leadbeateri Chrysochromulina simplex Chyrsochromulina cymbium Chrysochromulina campanulifera Chrysochromulina strobilus Calyptrosphaera radiata Oolithotus fragilis Umbilicosphaera hulburtiana Umbilicosphaera sibogae var. foliosa Calcidiscus leptoporus large Calcidiscus leptoporus intermediate Coccolithus pelagicus big Calyptrosphaera sp. 1 Cruciplacolithus neohelis cf. Jomonlithus littoralis Unidentified coccolithophorida Pleurochrysis sp. Reticulosphaera japonensis Ochrosphaera neapolitana Hymenomonas coronata Hymenomonas globosa Pleurochrysis carterae var. dentata Pleurochrysis sp. Pleurochrysis carterae Pleurochrysis elongata Pleurochrysis gayraliae Pleurochrysis sp. Algirosphaera robusta Scyphosphaera apsteinii Helicosphaera carteri var carteri Coronosphaera mediterranea Syracosphaera pulchra OLI 26041 OLI 510521 E. huxleyi /G. oceanica Dicrateria sp. Isochrysis litoralis Chrysotila lamellosa Pseudoisochrysis paradoxa Chyrsochromulina parkae Phaeocystis PLY 559 Phaeocystis jahnii Phaeocystis cordata Phaeocystis antarctica Phaeocystis pouchetii OLI 51004 Phaeocystis globosa OLI 16010 OLI 51080 OLI 26047 OLI 51076 (b) (c) C1 MA 200 B1

150

A 100

50 Y X B2

0 0,2 0,4 0,6 0,8 1 1,2 1,4 Distance to node

Fig. 4 Calculation of a molecular clock. (a) The ml tree according to Kooistra and Medlin (1996). From this regres- shown in Edvardsen et al. (2000) has been linearized sion line we have extrapolated the divergence of the warm- (Kooistra and Medlin 1996) so that all rates of evolution and cold-water Phaeocystis (Y) and the divergence of are the same. Fossil dates from coccolithophore taxa are P. pouchetii from P. antarctica (£) (solid circles on tree). placed on nodes where these taxa have their Wrst appear- (c) Temperature of Antarctic surface waters since the Cre- ance in the fossil record (open circles on tree). (b) A regres- taceous with the molecular tree plotted proportional to the sion of branch lengths against fossil dates has been performed time and the temperature, redrawn from Crame (1993) 123 10 Biogeochemistry (2007) 83:3–18 that the warm-water Phaeocystis species diverged strains have been examined with molecular tech- from the cold-water species approximately 30 Ma, niques so this is only a very preliminary suggestion. which coincides with the time that the Drake pas- Flagellated stages of P. pouchetii (Fig. 6a) sage opened and the ACC system was formed. were the subject of recent morphological studies This would have eVectively isolated ancestral (Jacobsen 2000, 2002). Cells are rounded, with an populations in the Antarctic suYciently to allow average diameter of 5
m. The Xagella are equal them to speciate from their warm-water ances- in length, ca 11
m, and heterodynamic. The tors. The separation of P. pouchetii from P. ant- haptonema is extremely short, 1–2
m, with a arctica is approximately 15 Ma, which coincides slight swelling, and is not easily seen with light with a major warming event in the world’s oceans microscopy. Body scales are of two types: almost at this time (Fig. 4). Before this time populations circular Xat plates, 0.24 £ 0.25
m, with raised must have been able to cross the equator from the rims, forming an external layer and smaller oval south to the north because water temperatures plates with slightly inXexed rims, 0.19 £ 0.15
m, were cool enough to allow survival, but this underneath the larger scales. Both types of scales warming event separated the two polar popula- show thin radiating ridges. Filaments (up to tions to allow them to diverge into the two species 30
m) arranged in groups of Wve with the typical we have today at the poles. Similar results have pentagonal proximal structure are seen outside been found for foraminfera (Darling et al. 2000, the cells, or are coiled up in vesicles under the cell 2004). surface. The presence of silica is reported in these Thus molecular data have deWned our species Wlaments (Jacobsen 2002). The ultrastructure is well and suggest which species are likely to be similar to that of P. globosa (Parke et al. 1971) composed of cryptic species. We detail below and of the other Phaeocystis for which this infor- basic descriptions of each of the formally mation is available (Zingone et al. 1999), with the described species and provide some indication as nucleus located posteriorly, the two chloroplasts to other undescribed species where this informa- with the embedded pyrenoids, and the Golgi body tion is known. between them. This cell stage can be infected by viruses (Jacobsen et al. 1996). P. globosa ScherVel (ScherVel 1900) forms Formally described species globular colonies with the cells evenly distributed throughout the colony (Fig. 5b). Molecular data An overview of the validly published taxa that and DNA content suggest that this is a complex of have been re-examined in recent years is pre- up to three or four cryptic species, but to date no sented in the following. These include species morphological investigations exist to support this. listed in the genus in its most recent review (Sour- Flagellated stages of P. globosa (Fig. 6b, c) nia 1988) and new species described after that were described for the Wrst time by Parke et al. date, with the exception of three taxa that have (1971) under the name of P. pouchetii, at the time not been studied since their description, P. amoe- when these two species were considered as stages boidea Büttner, P. sphaeroidea Büttner and within the life cycle of the same species. Cells are P. brucei Mangin. The Wrst two of these do not have 3–6
m, more frequently between 3 and 4.5
m. features characteristic of the genus, much the The two Xagella and the haptonema emerge from division Haptophyta, so it is likely that only the a depression in the cell body. Flagella are equal in latter species may still be a valid species of Phaeo- length, 1.5£ the cell length, and heterodynamic. cystis. The main distinctive characters of the spe- The haptonema is a quarter to a third the length cies included in this section are summarized in a of the Xagella. It is stiV and has a clear distal swell- table in Jacobsen (2002). ing. The haptonema is easily seen in live cells, P. pouchetii (Hariot in Pouchet) Lagerheim where it is directed forward while cells move. (Pouchet 1892) forms cloud-like colonies with cells Body scales show all radiating ridges on both sur- in packets of four (Fig. 5a). Molecular data suggest faces and are of two types: almost circular Xat that this is a species complex but here very few plates, 0.18 £ 0.19
m, with raised rims, forming

123 Biogeochemistry (2007) 83:3–18 11

Fig. 5 Light microscopic micrographs of colony stages of jahnii, (f) Phaeocystis sp.2 (a, b) taken from http://www.jo- Phaeocystis. (a) P. pouchetii, (b) P. globosa, (c) P. antarc- chemnet.de/Wu/OCB3043_21.html Scale bar = 100
m tica, young colony, (d) P. antarctica, older colony, (e) P. an external layer and smaller oval plates, point of view. It also forms globular colonies with 0.10 £ 0.13
m, with strongly inXexed rims, cells randomly distributed under the colony sur- underneath the larger scales. The ultrastructure is face (Fig. 5c, d). These colonies can become quite typical for the genus, with two golden-brown distorted and elongated with age. chloroplasts, with internal fusiform pyrenoids, Flagellated stages of P. antarctica (Fig. 6d) and some refringent vesicles probably including have received very little study. Only one illustra- storage products. The nucleus is posterior, tion of scales from an Antarctic Phaeocystis was whereas the Golgi body, with a high number of available (Larsen and Moestrup 1989), showing stacked cysternae, is seen in the space between oval scales of two diVerent sizes (0.27 £ 0.19
m the chloroplasts and the nucleus. The Xagellar and 0.18 £ 0.14
m, respectively). Recently, three bases have typical distal and proximal plates in diVerent morphs have been illustrated from Weld the transition zone. One of the two clones material from the Antarctic having scales that are observed by Parke et al. (1971) (clone 147) forms diVerent in size as compared to those shown by long Wlaments (up to 20
m) in groups of Wve Larsen and Moestrup and having a haptonema when discharged outside, with the proximal ends without a bulge on its tip (Marchant et al. 2005, arranged in a very typical pentagonal structure, Figs. 6f, 7d–f). Scales of still diVerent sizes have surrounded by a faint vesicle with a pore in the been detected in Xagellated stages obtained from centre. In the cells, the undischarged threads are the isolation of colonies, which are phylogeneti- found within a vesicle under the cell surface. cally close to SK 22 (Zingone and Montresor, Chrétiennot-Dinet et al. (1997) showed that these unpublished). The molecular data published to Wlaments contain alpha-chitin. date are derived only from colonial stages or from P. antarctica Karsten (Karsten 1905) is the Xagellate stages that were originally colonial. least known Phaeocystis from the morphological There is only a single type of ITS sequence pres-

123 12 Biogeochemistry (2007) 83:3–18

Fig. 6 Light microscopy (LM), transmission electron in the center of the Wve-Wlament structure, TEM, (j) P. cor- microscopy (TEM) and scanning electron microscopy data, SEM. (a) from Jacobsen (2002), (c) taken by Anna (SEM) micrographs of Xagellated stages of Phaeocystis. (a) Noordeloos, (d) taken by Dr. P. Assmy, (f) from Scott and P. pouchetii, TEM, (b) P. globosa, SEM, (c) P. globosa, Marchant (2005), (e, h, i) from Zingone et al. (1999), (b) LM, (d) P. antarctica, LM, (e) P. jahnii, TEM, (f) Phaeocys- and (g) from Vaulot et al. (1994). Scale bar = 1
m on (a, b, tis sp. from Antarctic waters TEM, (g) Phaeocystis sp. 3, g) Scale bar = 10
m on (c, d) Scale bar = 2
m on (e–j) SEM, (h) P. cordata TEM, (i) P. cordata, star-like pattern Scale bar = 0.3
m on (i)

123 Biogeochemistry (2007) 83:3–18 13

Fig. 7 LM, TEM and SEM micrographs of Xagellated stag- scrobiculata, (b, c) taken by Gandi Forlani, (d–f) from Scott es of Phaeocystis. (a) Phaeocystis sp. 1 (PML 559), LM, (b) and Marchant (2005). (g) From www.marbot.gu.se/SSS/ Phaeocystis sp. 1 (PML 559), SEM, (c) Tip of the tube-like others/Phaeocystis_scrobiculata.GIF. Scale bar = 10
m on structure ejected from Phaeocystis sp. 1 (PML 559), TEM. (a) Scale bar = 2
m on (b), (g) Scale bar = 0.5
m on (c–f) (d–f) Morphs 1, 2, 3 of P. antarctica, (g) Wlaments of P. ent in each strain in contrast to the multiple ITS among ITS sequences from Antarctic strains indi- variants in P. pouchetii and P. globosa, which cates that they could be all a single species, strongly suggests that colonial Phaeocystis from the whereas these new unicellular morphs in Weld sam- Antarctic are not a species complex. The similarity ples may belong to species as yet uncultivated

123 14 Biogeochemistry (2007) 83:3–18

(Fig. 7d–f). Alternatively, diVerent Xagellate mor- pole forward. Both larger and smaller scales are photypes could belong to diVerent sub-clades in oval, 0.25 £ 0.18
m and 0.18 £ 0.13
m, respec- the P. antarctica-clade. All this information indi- tively. The larger scales have upraised rims and a cates a high morphological diversity and suggests slight central knob, and form the external cell that there might be more than one species present investment. The smaller scales have inXexed rims in Phaeocystis from the Antarctic. Parallel mor- and form an inner layer adjacent to the plasma- phological investigations are warranted on strains lemma. The Wlaments are seen in disk-like vesi- belonging to distinct P. antarctica sub-clades. cles underneath the cell surface (up to three in a P. jahnii Zingone (Fig. 5e) forms colonies very cell) or discharged, with the typical Wve-ray star diVerent from all other Phaeocystis colonies pattern (Fig 6i). Ultrathin sections show the two (Zingone et al. 1999). These are loose aggregates Xagella and the haptonema inserted along a line of non-motile cells embedded in a sticky mucilag- that is transversal to the plane crossing the plast- inous matrix probably of polysaccharide nature, ids. Comparable information is not available for with no external layer nor a deWnite shape. In cul- other species yet. The internal microanatomy is ture material the colonies may form wide sheets similar to that of the other species of the genus. with margins at times sticking to the cell tube. P. scrobiculata Moestrup (Fig. 7g) was Colonial cells range from 6 to 8.5
m and have 2– described from Weld material collected in New 4 chloroplasts. Zealand waters (Moestrup 1979) as a unicell. Flagellated cells of P. jahnii (Fig. 6e) are There is no evidence that it makes colonies nor rounded, 3.5–5
m diameter, with Xagella of mark- any molecular work has been done on it. Its cells edly unequal length (8.5–12
m and 5.5–6.5
m, are 8
m in diameter with two types of scales, respectively). The haptonema is relatively long 0.6 £ 0.45
m and 0.19 £ 0.21
m in size. Both (3–4.5
m) and without a marked bulge at the types of scales are structureless on the dorsal side, end. As compared to the other Phaeocystis spe- but with ridges radiating from a plain centre on cies, scales are thinner and more delicate, with a the ventral side. Its Xagella and haptonema are very faint radiating pattern lacking in the central twice the length found in P. globosa and the part of the scale. The larger scales (0.35 £ 0.28
m) scales are about two times larger. Another distin- do not have an upraised rim, whereas the smaller guishing feature is the Wlaments that it produces, underlying scales (0.18 £ 0.14
m) have the which are in groups of nine (eight pairs and one typical inXexed rim. A refringent yellow-orange single), in contrast to the production of Wve single body is often seen in the live cells in the space Wlaments from the other species that produce Wla- between the chloroplasts. Filaments have not ments (Fig. 7g). The centre pattern of the Wla- been observed in this species. ments is rather irregular and does not form the P. cordata Zingone et Chrétiennot-Dinet characteristic star shape in the middle. Filaments (Fig. 6h–j) occurs only as single cells which are arranged with the same pattern have also been typically triangular, heart-shaped or oval, some- found in Australian waters (HallegraeV 1983) and what Xattened, with a deep Xagellar depression in the Mediterranean Sea (Zingone et al. 1999). and more or less pointed antapical end (Zingone However, scales were smaller in both Australian et al. 1999). The average size is 3–3.5
m long, and Mediterranean specimens, which suggests a 3–4
m wide, and ca. 2.5
m thick. The two Xagella possible higher diversity to be explored within are slightly subequal, 5.5–7.5 and 4.5–6
m length, this taxon as well. respectively. The haptonema is very short (2.2–2.5
m) and hardly visible in light micros- copy, with a bulging end observed in the electron Undescribed species microscope. Cells generally swim with the Xagel- lar pole directed backwards, and the two Xagella In addition to the species described in the litera- straight, completely hiding the haptonema. Cells ture, a number of taxa ascribed to Phaeocystis that rotate around their longitudinal axis while mov- are currently under morphological and molecular ing. Rarely cells are seen moving with the Xagellar investigation are presented in the following.

123 Biogeochemistry (2007) 83:3–18 15

Phaeocystis sp. 1 (PML 559) (Fig. 7a–c) seems Phaeocystis Lagerheim 1893, Zingone and only to be present in single cells. The two Xagella Medlin emended. are 8.5–12
m and 5.5–6.5
m, respectively. The Motile cells with two more or less equal Xagella haptonema is 3–4.5
m long, without a bulge at and a shorter non-coiling haptonema; 1–4 parietal the end. The larger scales are similar to those of chloroplasts; cell body often covered with Xat P. cordata, though larger (ca. 0.35 £ 0.22
m), scales of two diVerent sizes. Ejectile organelles with thick upraised rim and a central knob. known for several species. Complex life cycles Smaller scales (0.25 £ 0.17
m) have inXexed involving the formation of non-motile stages, not rims. An unusual feature of this species is that it known for all species. Non-motile cells usually produces tube-like structures with peculiar ends without appendages and scales, either single or that are ejected from the cell. These bodies may arranged in spherical, lobed, sheathed or irregular be present in number of 5–7 per cell (Fig. 7b) and gelatinous colonies; if appendages present, usu- leave a large depression once extruded. Many ally shorter or incomplete. benthic stages are formed as the culture ages and it is likely that the tube-like bodies help to attach the cells to the substrate. Outlook Phaeocystis sp. 2 (Fig. 5f) is the only Phaeocys- tis so far cultivated from the Mediterranean Sea From the observations we have to date, including that has been shown to form typical colonies of Weld and cultured material and molecular data, it spherical shape (Zingone, Borra, Forlani and Pro- is clear that we have come a long way from just caccini, in preparation). The Xagellates have an 10 years ago, when we had only one species of irregular shape, with pronounced shoulders at the Phaeocystis: P. globosa with a cosmopolitan dis- Xagellar pole. The Xagella are markedly unequal tribution. We now have a much clearer picture of in length, the haptonema has no bulging end. No the species in the genus and their distribution. scales were ever detected on the cell surface, nor However Phaeocystis still holds many mysteries. any kinds of Wlaments. 18S analyses demonstrate Clearly, there are more species of Phaeocystis that this taxon belongs to the P. globosa clade, than presently formally recognized. Some of these although it diVers by nine base pairs, a diVerence are morphologically distinct, whereas others that is comparable to that between P. pouchetii require further research to assess whether they and P. antarctica. ITS sequence is unalignable are cryptic species or, rather, they are morpholog- with those of those available for the other ically distinct at least in some stages of their life P. globosa strains. cycle. New avenues of molecular and morphologi- Phaeocystis sp. 3 (Fig. 6g) includes strains iso- cal investigation concern the taxa known only lated from the North-Western Mediterranean Sea. from Weld material, such as the three morpho- Being single-celled and similar to P. cordata in types of P. antarctica, and the as yet uncultured scale morphology, it was preliminarily attributed and rare P. scrobiculata, or the Xagellate with to the latter species (as strains MEDNS2 and cup-shaped plates from South African waters MEDNS3 in Zingone et al. 1999), but it has mor- (Pienaar 1991, 1996). As Xagellate stages appear phological diVerences that were initially unappre- to be more widespread and diverse as compared ciated. As compared to P. cordata, Phaeocystis sp. to colonial stages, material to study should be 3 is somewhat larger, has a rounded body, shorter gathered through speciWc cultivation techniques Xagella and the larger body scales are almost cir- (e.g., serial dilution techniques). Whereas the cular rather than oval. Preliminary molecular anal- function of the thin Wlaments has not been fully ysis has placed it within the P. globosa complex. clariWed, the role of the peculiar extrusomes Clearly, morphological details of the species found in PLY 559 is even more diYcult to under- encountered in recent years fall outside of the stand. Presumably these are diVerent attachment original description of the genus Phaeocystis, mechanisms, but they could also be involved in therefore we feel it necessary to emend the genus potential overwintering stage formation (Gäbbler description as follows: et al. unpublished observations). The molecular

123 16 Biogeochemistry (2007) 83:3–18 tools that have been used so far have signiWcantly Chang FH (1983) The mucilage producing Phaeocystis contributed to delineate Phaeocystis species. pouchetii (Prymnesiophyceae) cultured from the W 1981 ‘Tasman Bay slime’. N Z J Mar Freshw Res What remains to be clari ed is the genetic diver- 17:165–168 sity within the major species and how this diver- Chrétiennot-Dinet MJ, Giraud-Guille M-M, Vaulot D, sity changes in time and space, which will require Putaux J-L, Saito Z, Chanzy H (1997) The chitinous W the set up of new high-resolution methods (see nature of the laments ejected by Phaeocystis (Prym- nesiophyceae). J Phycol 33:666–672 Gäbbler et al. (2007)) for the latest developments Crame JA (1993) Latitudinal range Xuctuations in the ma- in population genetic analysis of Phaeocystis). rine realm through geological times. Trends Ecol Evol This information, coupled with a better circum- 8:162–166 scription of species, is the prerequisite for signiW- Chase MW, Knapp S, Cox AV, Clarkson JJ, Butsko Y, Jo- seph J, Savolainen V, Parokonny AS 2003. Molecular cant advancements in the understanding of the systematics, GISH and the origin of hybrid taxa in ecology of one of the key players of the world Nicotiana (Solanaceae). Ann Bot 92:107–127 ocean’s plankton. Darling KF, Wade CM, Stewart IA, Kroon D, Dingle R, Brown AJL (2000) Molecular evidence for genetic Acknowledgements Dr. Philipp Assmy kindly provided mixing of Arctic and Antarctic subpolar populations photographs of P. antarctica. Gandi Forlani provided pho- of plankton foraminifers. Nature 405:43–47 tographs of Phaeocystis sp. 1 (PML 559). Photographs tak- Darling KF, Kucera M, Pudsey CJ, Wade CM (2004) W en from Fig. 5.2 from Scott and Marchant (2005) were Molecular evidence links cryptic diversi cation in po- reproduced with permission from F.J. Scott and H.J. lar planktonic protists to Quaternary climate dynam- Marchant (Eds), Antarctic Marine Protists 258, (2005), ics. PNAS 101:7657–7662 Copyright Australian Biological Resources Study, Australian Davidson AT (1985) Aspects of the biology of Phaeocystis Antarctic Division and Andrew Davidson. Figures repro- pouchetii (Prymnesiophyceae) (Hons. Thesis). duced from ‘Morphology, relative DNA content and University of Tasmania hypothetical life cycle of Phaeocystis pouchetii (Prymnesi- Davidson AT, Marchant H (1992) The biology and ecology ophyceae); with special emphasis on the Xagellated cell of Phaeocystis (Prymnesiophyceae). In: Round FE, type’ by Jacobsen (2002) from Sarsia, www.tandf.no/sarsia, Chapman DJ (eds) Progress in phycological research, 2002, 87: 338–349, by permission of Taylor and Francis AS. vol. 8. Biopress, Bristol, pp 1–45 Figures 2a, g in Vaulot et al. (1994) and Fig. 6, 9, 32 in Edvardsen B, Eikrem W, Green JC, Andersen RA, Moon- Zingone et al. (1999) were reproduced with permission of Van Der Staay SY, Medlin LK (2000). Phylogenetic the Phycological Society of America. This review falls within reconstructions of the Haptophyta inferred from the scopes of the EU Network of Excellence MARBEF rRNA sequences and available morphological data. (Marine Biodiversity and Ecosystem Functioning). Phycologia 39:19–35 Fevolden SE, Schneppenheim R (1989) Genetic homoge- neity of krill (Euphausia superba Dana) in the South- ern Ocean. Polar Biol 9:533–539 References Gäbbler S, Hayes PK, Medlin LK (2007) Methods used to reveal genetic diversity in the colony forming prymne- Bätje M, Michaelis H (1986) Phaeocystis pouchetii blooms siophytes Phaeocystis antarctica, P. globosa and P. in the east Frisian coastal waters (German Bight, pouchetii––preliminary results. Biogeochemistry (this North Sea). 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