DESCRIPTION OF THE PHYLUM HAPTOMONADA (MARGULIS AND SCHWARTZ 1998)

EUKARYA> CHROMALVEOLATA> HACROBIAE> HAPTOMONADA

Haptomonada (hap-to-mo-NA-da) is made of two Greek roots that mean hold (hapto -άπτω); and unit (monada -μονάδα). The reference is to a cell (a unit) with a holding structure, which is the haptonema (text with tooltip) A haptonema is a flagellum-like structure that characterizes the Haptotista. The formula for the axonemal microtubular array is 6(1)+0. Usually functions as a holdfast. .

INTRODUCTION TO THE HAPTOMONADA The haptophytes, coccolithophorids, or prymnesiophytes are important marine phytoplankters that, in the motile form, have a unicell with two whiplash flagella (text with tooltip) (1) A whiplash flagellum is a eukaryotic 9+2 flagellum with few or no flagellar hairs or scales. These may be directed anteriorly or posteriorly. (2) A whiplash flagellum is free of hair-like mastigonemes and usually is trailing or posteriorly-directed. and a covering of delicate calcium carbonate scales called coccoliths (Figures 1 and 2). Another defining feature is the presence of a haptonema (Figure 3), a flagellum-like structure (thus the name of the group). Pavlova (Figure 4) differs from the other haptomonads in that it has unequal, heterodynamic flagella (text with tooltip) Heterodynamic flagella occur on the same cell but beat with different patterns (e.g. anterior-posterior). , a flagellar swelling (text with tooltip) A flagellar swelling is a portion of the base of a flagellum that usually is light sensitive (as in the eyespot apparatus of euglenoids). , and an eyespot (text with tooltip) An eyespot is a light-sensitive structure that does not form an image. This can be part of an organelle as in the chloroplast of certain microbial eukaryotes. It can be an elaborate structure that involves a light-sensitive swelling at the base of a flagellum (as in the euglenoids) or it can be a multicellular structure as in planarians. . Emiliania huxleyi is one of the most successful species on the planet. It can form huge blooms in the North Atlantic that are larger than most countries. Despite its importance, little is known if its biology. Green et al. (1996) described the life history of the cell and showed that the coccolith-bearing C cell (see Figure 5) is diploid while the motile scale-bearing S cell is haploid. The presumption is that the S cell is a gamete. The N cell is completely naked and non-motile. Green et al. (1996) claim that all three forms C, S, and N can replicate themselves. However, more recent work (e.g. Laguna et al. 2001, Billard and Inouye 2004) suggest that the N cell may be a developmental stage to an S, but its role remains unknown. Morin (2008) and Frada et al. (2008) suggest that the modulation between S and C (haploid and diploid) phases might help to mask the cells from viruses which can wipe out a bloom and make the ocean white with dispersed coccoliths.

FIGURE 1. Cells of Isochrysis showing the variable form of the cell, the anteriorly-directed (text with tooltip) An anteriorly-directed flagellum extends in the direction of the motion of the motile cell. The interpretation is that the flagellum functions by pulling the cell. equal flagella, and the two chromoplasts (text with tooltip) Chromoplast is the general term for a photosynthetic organelle. Technically, a chloroplast is a particular chromoplast in which the dominant chlorophylls are A and B. . Image from http://www.nhm.ac.uk/hosted_sites/ina/CODENET/galleries/DICimages/source/iso.htm	FIGURE 2. An SEM micrograph of the diploid phase ( sporophyte (text with tooltip) A sporophyte is the diploid phase of an organism that exhibits alternation of generation. This phase produces spores usually in specialized sporangia as the immediate products of meiosis. ) of a fossil Coccolithus showing the scale-like coccoliths. Image from http://www.ucl.ac.uk/GeolSci/micropal/calcnanno.html	FIGURE 3. Chrysochromulina displaying the paired flagella and short haptonema between them. Image from http://www.biol.tsukuba.ac.jp/~inouye/ino/h/prym.gif	FIGURE 4. Pavlova, unlike other haptomonads, has two unequal heterodynamic flagella. Image from http://www.reed-mariculture.com/microalgae/pav-100X.jpg

FIGURE 5. Diagram of Emiliania huxleyi life cycle. C-cells are non-motile and covered with coccoliths (similar to Figure 2). The S-cells are covered with scales and are motile (similar to Figure 3). Green et al. (1996) demonstrated that S-cells are haploid and therefore likely can function as gametes. The role that the non-motile N-cell plays in the life cycle is unknown. Figure from Green et al. (1996).

Some members of this group have a life cycle that alternates between a prostrate haploid filament (gametophyte) and a globose motile diploid sporophyte. The gametophyte produces isogametes that fuse to make the sporophyte. Likely most have such a life cycle, but the gametophyte is cryptic or identified as something completely different. Members of this phylum are not restricted to marine environments. Chrysochromulina (Figure 3), a tiny freshwater form is quite common in certain ponds and lakes. In one sample, I collected a concentration of around 35,000 cells per milliliter in an acid-sensitive pond in central Pennsylvania. Lovelock (1991) argues that the haptophytes may be responsible for the capture and removal of significant amounts of atmospheric carbon by the deposition of their scales in the ocean. He also argues that haptophytes release sulfur compounds into the air that induce the formation of clouds and increase the albedo of the planet. This system is based on Green et al. (1990), Margulis and Schwartz (1988, Pr-5 and 1998, Pr-10) and Sleigh et al. (1985) in which the haptophytes (or prymnesiophytes) are given phylum-level status. Systematic treatments of the haptophytes have been quite varied. Bold and Wynne (1985), Sze (1986), and Lee (1980) consider the haptophytes to occupy a class within the chrysophyte complex. Grell (1973), Kudo (1966) and Lee et al. (1985) treat the haptophytes as a separate order associated with the chrysophytes and within the phytomonads. Taylor (1976) shows the haptophytes as a group which is very closely related to the chrysophytes. The analyses of Dodge (1973) are inconclusive; one shows the haptophytes within the chrysophyte complex while another analysis shows the haptophytes related to the chlorophytes. Hibberd (1980) and Lee et al. (1985) beg the question of haptophyte taxonomy. Patterson (1999) recognizes the haptophytes as a natural group with no known affinities. Baldauf (2003a) presents a consensus view of recent molecular-ultrastructural data in which the haptophytes occur in a clade with the cryptophytes and are associated with the heterokont clade. That has been confirmed by Hackett et al. (2007) and Burki et al. (2007, 2009) with varying associations with the Heterokont+Alveolate+Rhizaria groups. Analyses of Burki et al. (2009) and Okamoto et al. (2009) confirm that the haptophytes together with cryptophytes and centrohelids form a monophyletic group that they call Hacrobia (this is equivalent to our kingdom-level taxon, Eukaryomonadae). The analysis of Hampl et al. (2009), in their comparison of 143 proteins for 48 taxa that encompassed the supergroups of the eukaryotes, challenges the Hacrobia hypothesis and suggests that the haptomonads are sisters to or emerge from within the Archaeplastida while the cryptomonads remain associated with the chromalveolates. Burki et al. (2012) found that the cryptomonads emerged with the plants while the haptophytes were basal in the chromalveolates. While these two groups remain problematic, we will use the Hacrobia hypothesis in associating the cryptomonads, centrohelids and haptomonads as a group associated with the chromalveolates. Figure 6 shows a molecular phylogeny based on Hsp90 (Okamoto et al. 2009), but the three taxa can emerge in any of the three possible topologies with other molecular analyses (e.g. LSU, SSU, genomic comparisons; Okamoto et al. 2009 and Burki et al. 2009). Because of the unique set of characters (e.g. haptonema, calcium carbonate scales, most with a pair of anteriorly-directed whiplash flagella, and a unique golgi organization), we have separated the haptophytes into their own phylum, Haptomonada, which has 2 classes.

FIGURE 6. A cladogram showing the relationship of the haptomonad classes (taxa in shaded box) with the rest of the Hacrobia (taxa in bold). The relationship is a simplified view of the molecular phylogeny generated by Okamoto et al. (2009) based on Hsp90.

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By Jack R. Holt. Last revised: 03/03/2013