Fig. 4 Calculation of a molecular clock. (a) The ml tree shown in Edvardsen et al. (2000) has been linearized (Kooistra and Medlin 1996) so that all rates of evolution are the same. Fossil dates from coccolithophore taxa are placed on nodes where these taxa have their Wrst appearance in the fossil record (open circles on tree). (b) A regression of branch lengths against fossil dates has been performed according to Kooistra and Medlin (1996). From this regression line we have extrapolated the divergence of the warm-and cold-water Phaeocystis (Y) and the divergence of P. pouchetii from P. antarctica (x) (solid circles on tree). (c) Temperature of Antarctic surface waters since the Cretaceous with the molecular tree plotted proportional to the time and the temperature, redrawn from Crame (1993)
that the warm-water Phaeocystis species diverged from the cold-water species approximately 30 Ma, which coincides with the time that the Drake passage opened and the ACC system was formed. This would have effectively isolated ancestral populations in the Antarctic sufficiently to allow them to speciate from their warm-water ancestors. The separation of P. pouchetii from P. antarctica is approximately 15 Ma, which coincides with a major warming event in the world's oceans at this time (Fig. 4). Before this time populations must have been able to cross the equator from the south to the north because water temperatures were cool enough to allow survival, but this warming event separated the two polar populations to allow them to diverge into the two species we have today at the poles. Similar results have been found for foraminfera (Darling et al. 2000, 2004).
Thus molecular data have defined our species well and suggest which species are likely to be composed of cryptic species. We detail below basic descriptions of each of the formally described species and provide some indication as to other undescribed species where this information is known.
An overview of the validly published taxa that have been re-examined in recent years is presented in the following. These include species listed in the genus in its most recent review (Sour-nia 1988) and new species described after that date, with the exception of three taxa that have not been studied since their description, P. amoe-boidea Büttner, P. sphaeroidea Büttner and P. brucei Mangin. The first two of these do not have features characteristic of the genus, much the division Haptophyta, so it is likely that only the latter species may still be a valid species of Phaeocystis. The main distinctive characters of the species included in this section are summarized in a table in Jacobsen (2002).
P. pouchetii (Hariot in Pouchet) Lagerheim (Pouchet 1892) forms cloud-like colonies with cells in packets of four (Fig. 5a). Molecular data suggest that this is a species complex but here very few strains have been examined with molecular techniques so this is only a very preliminary suggestion.
Flagellated stages of P. pouchetii (Fig. 6a) were the subject of recent morphological studies (Jacobsen 2000, 2002). Cells are rounded, with an average diameter of 5 im. The flagella are equal in length, ca 11 |m, and heterodynamic. The haptonema is extremely short, 1-2 |m, with a slight swelling, and is not easily seen with light microscopy. Body scales are of two types: almost circular flat plates, 0.24 x 0.25 |m, with raised rims, forming an external layer and smaller oval plates with slightly inflexed rims, 0.19 x 0.15 |m, underneath the larger scales. Both types of scales show thin radiating ridges. Filaments (up to 30 |m) arranged in groups of five with the typical pentagonal proximal structure are seen outside the cells, or are coiled up in vesicles under the cell surface. The presence of silica is reported in these filaments (Jacobsen 2002). The ultrastructure is similar to that of P. globosa (Parke et al. 1971) and of the other Phaeocystis for which this information is available (Zingone et al. 1999), with the nucleus located posteriorly, the two chloroplasts with the embedded pyrenoids, and the Golgi body between them. This cell stage can be infected by viruses (Jacobsen et al. 1996).
P. globosa Scherffel (Scherffel 1900) forms globular colonies with the cells evenly distributed throughout the colony (Fig. 5b). Molecular data and DNA content suggest that this is a complex of up to three or four cryptic species, but to date no morphological investigations exist to support this.
Flagellated stages of P. globosa (Fig. 6b, c) were described for the first time by Parke et al. (1971) under the name of P. pouchetii, at the time when these two species were considered as stages within the life cycle of the same species. Cells are 3-6 |m, more frequently between 3 and 4.5 |m. The two Xagella and the haptonema emerge from a depression in the cell body. Flagella are equal in length, 1.5x the cell length, and heterodynamic. The haptonema is a quarter to a third the length of the Xagella. It is stiV and has a clear distal swelling. The haptonema is easily seen in live cells, where it is directed forward while cells move. Body scales show all radiating ridges on both surfaces and are of two types: almost circular Xat plates, 0.18 x 0.19 |m, with raised rims, forming
an external layer and smaller oval plates, 0.10 x 0.13 |m, with strongly inflexed rims, underneath the larger scales. The ultrastructure is typical for the genus, with two golden-brown chloroplasts, with internal fusiform pyrenoids, and some refringent vesicles probably including storage products. The nucleus is posterior, whereas the Golgi body, with a high number of stacked cysternae, is seen in the space between the chloroplasts and the nucleus. The flagellar bases have typical distal and proximal plates in the transition zone. One of the two clones observed by Parke et al. (1971) (clone 147) forms long filaments (up to 20 |m) in groups of five when discharged outside, with the proximal ends arranged in a very typical pentagonal structure, surrounded by a faint vesicle with a pore in the centre. In the cells, the undischarged threads are found within a vesicle under the cell surface. Chretiennot-Dinet et al. (1997) showed that these filaments contain alpha-chitin.
P. antarctica Karsten (Karsten 1905) is the least known Phaeocystis from the morphological point of view. It also forms globular colonies with cells randomly distributed under the colony surface (Fig. 5c, d). These colonies can become quite distorted and elongated with age.
Flagellated stages of P. antarctica (Fig. 6d) have received very little study. Only one illustration of scales from an Antarctic Phaeocystis was available (Larsen and Moestrup 1989), showing oval scales of two different sizes (0.27 x 0.19 im and 0.18 x 0.14 |m, respectively). Recently, three different morphs have been illustrated from field material from the Antarctic having scales that are diVerent in size as compared to those shown by Larsen and Moestrup and having a haptonema without a bulge on its tip (Marchant et al. 2005, Figs. 6f, 7d-f). Scales of still different sizes have been detected in flagellated stages obtained from the isolation of colonies, which are phylogeneti-cally close to SK 22 (Zingone and Montresor, unpublished). The molecular data published to date are derived only from colonial stages or from flagellate stages that were originally colonial. There is only a single type of ITS sequence pres-
Fig. 6 Light microscopy (LM), transmission electron microscopy (TEM) and scanning electron microscopy (SEM) micrographs of flagellated stages of Phaeocystis. (a) P. pouchetii, TEM, (b) P. globosa, SEM, (c) P. globosa, LM, (d) P. antarctica, LM, (e) P. jahnii, TEM, (f) Phaeocystis sp. from Antarctic waters TEM, (g) Phaeocystis sp. 3, SEM, (h) P. cordata TEM, (i) P. cordata, star-like pattern
Fig. 6 Light microscopy (LM), transmission electron microscopy (TEM) and scanning electron microscopy (SEM) micrographs of flagellated stages of Phaeocystis. (a) P. pouchetii, TEM, (b) P. globosa, SEM, (c) P. globosa, LM, (d) P. antarctica, LM, (e) P. jahnii, TEM, (f) Phaeocystis sp. from Antarctic waters TEM, (g) Phaeocystis sp. 3, SEM, (h) P. cordata TEM, (i) P. cordata, star-like pattern in the center of the five-filament structure, TEM, (j) P. cordata, SEM. (a) from Jacobsen (2002), (c) taken by Anna Noordeloos, (d) taken by Dr. P. Assmy, (f) from Scott and Marchant (2005), (e, h, i) from Zingone et al. (1999), (b) and (g) from Vaulot et al. (1994). Scale bar = 1 ^m on (a, b, g) Scale bar = 10 ^m on (c, d) Scale bar = 2 ^m on (e-j) Scale bar = 0.3 ^m on (i)
ent in each strain in contrast to the multiple ITS variants in P. pouchetii and P. globosa, which strongly suggests that colonial Phaeocystis from the Antarctic are not a species complex. The similarity scrobiculata, (b, c) taken by Gandi Forlani, (d-f) from Scott and Marchant (2005). (g) From www.marbot.gu.se/SSS/ others/Phaeocystis_scrobiculata.GIF. Scale bar = 10 pm on (a) Scale bar = 2 pm on (b), (g) Scale bar = 0.5 pm on (c-f)
among ITS sequences from Antarctic strains indicates that they could be all a single species, whereas these new unicellular morphs in field samples may belong to species as yet uncultivated
(Fig. 7d-f). Alternatively, different flagellate morphotypes could belong to different sub-clades in the P. antarctica-clade. All this information indicates a high morphological diversity and suggests that there might be more than one species present in Phaeocystis from the Antarctic. Parallel morphological investigations are warranted on strains belonging to distinct P. antarctica sub-clades.
P. jahnii Zingone (Fig. 5e) forms colonies very different from all other Phaeocystis colonies (Zingone et al. 1999). These are loose aggregates of non-motile cells embedded in a sticky mucilaginous matrix probably of polysaccharide nature, with no external layer nor a definite shape. In culture material the colonies may form wide sheets with margins at times sticking to the cell tube. Colonial cells range from 6 to 8.5 |m and have 24 chloroplasts.
Flagellated cells of P. jahnii (Fig. 6e) are rounded, 3.5-5 im diameter, with flagella of markedly unequal length (8.5-12 |m and 5.5-6.5 |m, respectively). The haptonema is relatively long (3-4.5 im) and without a marked bulge at the end. As compared to the other Phaeocystis species, scales are thinner and more delicate, with a very faint radiating pattern lacking in the central part of the scale. The larger scales (0.35 x 0.28 im) do not have an upraised rim, whereas the smaller underlying scales (0.18 x 0.14 |m) have the typical inflexed rim. A refringent yellow-orange body is often seen in the live cells in the space between the chloroplasts. Filaments have not been observed in this species.
P. cordata Zingone et Chretiennot-Dinet (Fig. 6h-j) occurs only as single cells which are typically triangular, heart-shaped or oval, somewhat flattened, with a deep flagellar depression and more or less pointed antapical end (Zingone et al. 1999). The average size is 3-3.5 im long, 3-4 |m wide, and ca. 2.5 im thick. The two flagella are slightly subequal, 5.5-7.5 and 4.5-6 |m length, respectively. The haptonema is very short (2.2-2.5 |m) and hardly visible in light microscopy, with a bulging end observed in the electron microscope. Cells generally swim with the flagellar pole directed backwards, and the two flagella straight, completely hiding the haptonema. Cells rotate around their longitudinal axis while moving. Rarely cells are seen moving with the flagellar pole forward. Both larger and smaller scales are oval, 0.25 x 0.18 |m and 0.18 x 0.13 |m, respectively. The larger scales have upraised rims and a slight central knob, and form the external cell investment. The smaller scales have inflexed rims and form an inner layer adjacent to the plasmalemma. The filaments are seen in disk-like vesicles underneath the cell surface (up to three in a cell) or discharged, with the typical five-ray star pattern (Fig6i). Ultrathin sections show the two flagella and the haptonema inserted along a line that is transversal to the plane crossing the plast-ids. Comparable information is not available for other species yet. The internal microanatomy is similar to that of the other species of the genus.
P. scrobiculata Moestrup (Fig. 7g) was described from field material collected in New Zealand waters (Moestrup 1979) as a unicell. There is no evidence that it makes colonies nor any molecular work has been done on it. Its cells are 8 im in diameter with two types of scales, 0.6 x 0.45 |m and 0.19 x 0.21 |m in size. Both types of scales are structureless on the dorsal side, but with ridges radiating from a plain centre on the ventral side. Its flagella and haptonema are twice the length found in P. globosa and the scales are about two times larger. Another distinguishing feature is the filaments that it produces, which are in groups of nine (eight pairs and one single), in contrast to the production of five single filaments from the other species that produce filaments (Fig. 7g). The centre pattern of the filaments is rather irregular and does not form the characteristic star shape in the middle. Filaments arranged with the same pattern have also been found in Australian waters (Hallegraeff 1983) and in the Mediterranean Sea (Zingone et al. 1999). However, scales were smaller in both Australian and Mediterranean specimens, which suggests a possible higher diversity to be explored within this taxon as well.
In addition to the species described in the literature, a number of taxa ascribed to Phaeocystis that are currently under morphological and molecular investigation are presented in the following.
Phaeocystis sp. 1 (PML 559) (Fig. 7a-c) seems only to be present in single cells. The two flagella are 8.5-12 | m and 5.5-6.5 | m, respectively. The haptonema is 3-4.5 | m long, without a bulge at the end. The larger scales are similar to those of P. cordata, though larger (ca. 0.35 x 0.22 | m), with thick upraised rim and a central knob. Smaller scales (0.25 x 0.17 im) have inflexed rims. An unusual feature of this species is that it produces tube-like structures with peculiar ends that are ejected from the cell. These bodies may be present in number of 5-7 per cell (Fig. 7b) and leave a large depression once extruded. Many 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.
Phaeocystis sp. 2 (Fig. 5f) is the only Phaeocys-tis so far cultivated from the Mediterranean Sea that has been shown to form typical colonies of spherical shape (Zingone, Borra, Forlani and Pro-caccini, in preparation). The flagellates have an irregular shape, with pronounced shoulders at the flagellar pole. The flagella are markedly unequal in length, the haptonema has no bulging end. No scales were ever detected on the cell surface, nor any kinds of filaments. 18S analyses demonstrate that this taxon belongs to the P. globosa clade, although it diVers by nine base pairs, a diVerence that is comparable to that between P. pouchetii and P. antarctica. ITS sequence is unalignable with those of those available for the other P. globosa strains.
Phaeocystis sp. 3 (Fig. 6g) includes strains isolated from the North-Western Mediterranean Sea. Being single-celled and similar to P. cordata in scale morphology, it was preliminarily attributed to the latter species (as strains MEDNS2 and MEDNS3 in Zingone et al. 1999), but it has morphological diVerences that were initially unappreciated. As compared to P. cordata, Phaeocystis sp. 3 is somewhat larger, has a rounded body, shorter flagella and the larger body scales are almost circular rather than oval. Preliminary molecular analysis has placed it within the P. globosa complex.
Clearly, morphological details of the species encountered in recent years fall outside of the original description of the genus Phaeocystis, therefore we feel it necessary to emend the genus description as follows:
Phaeocystis Lagerheim 1893, Zingone and Medlin emended.
Motile cells with two more or less equal flagella and a shorter non-coiling haptonema; 1-4 parietal chloroplasts; cell body often covered with flat scales of two different sizes. Ejectile organelles known for several species. Complex life cycles involving the formation of non-motile stages, not known for all species. Non-motile cells usually without appendages and scales, either single or arranged in spherical, lobed, sheathed or irregular gelatinous colonies; if appendages present, usually shorter or incomplete.
From the observations we have to date, including field and cultured material and molecular data, it is clear that we have come a long way from just 10 years ago, when we had only one species of Phaeocystis: P. globosa with a cosmopolitan distribution. We now have a much clearer picture of the species in the genus and their distribution. However Phaeocystis still holds many mysteries. Clearly, there are more species of Phaeocystis than presently formally recognized. Some of these are morphologically distinct, whereas others require further research to assess whether they are cryptic species or, rather, they are morphologically distinct at least in some stages of their life cycle. New avenues of molecular and morphological investigation concern the taxa known only from field material, such as the three morphotypes of P. antarctica, and the as yet uncultured and rare P. scrobiculata, or the flagellate with cup-shaped plates from South African waters (Pienaar 1991, 1996). As flagellate stages appear to be more widespread and diverse as compared to colonial stages, material to study should be gathered through specific cultivation techniques (e.g., serial dilution techniques). Whereas the function of the thin filaments has not been fully clarified, the role of the peculiar extrusomes found in PLY 559 is even more difficult to understand. Presumably these are diVerent attachment mechanisms, but they could also be involved in potential overwintering stage formation (Gabbler et al. unpublished observations). The molecular tools that have been used so far have significantly contributed to delineate Phaeocystis species. What remains to be clarified is the genetic diversity within the major species and how this diversity changes in time and space, which will require the set up of new high-resolution methods (see Gabbler et al. (2007)) for the latest developments in population genetic analysis of Phaeocystis). This information, coupled with a better circumscription of species, is the prerequisite for significant advancements in the understanding of the ecology of one of the key players of the world ocean's plankton.
Acknowledgements Dr. Philipp Assmy kindly provided photographs of P. antarctica. Gandi Forlani provided photographs of Phaeocystis sp. 1 (PML 559). Photographs taken from Fig. 5.2 from Scott and Marchant (2005) were reproduced with permission from F.J. Scott and H.J. Marchant (Eds), Antarctic Marine Protists 258, (2005), Copyright Australian Biological Resources Study, Australian Antarctic Division and Andrew Davidson. Figures reproduced from 'Morphology, relative DNA content and hypothetical life cycle of Phaeocystis pouchetii (Prymnesi-ophyceae); with special emphasis on the Xagellated cell type' by Jacobsen (2002) from Sarsia, www.tandf.no/sarsia, 2002, 87: 338-349, by permission of Taylor and Francis AS. Figures 2a, g in Vaulot et al. (1994) and Fig. 6, 9, 32 in Zingone et al. (1999) were reproduced with permission of the Phycological Society of America. This review falls within the scopes of the EU Network of Excellence MARBEF (Marine Biodiversity and Ecosystem Functioning).
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Biogeochemistry (2007) 83:19-27 DOI 10.1007/s10533-007-9084-4
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