J. Phycol. 47, 2–4 (2011)
2011 Phycological Society of America
DOI: 10.1111/j.1529-8817.2010.00951.x
CHARACTERIZATION OF THE PARMALES: MUCH MORE THAN THE RESOLUTION
OF A TAXONOMIC ENIGMA
On the eve of the ‘‘sixth mass extinction’’ in
Earth’s history, phycologists face challenging questions on the role and the fate of algae, one of the
most important groups of primary producers on the
planet. This task is far from trivial, particularly given
that it is likely that a majority of algal species are
still unknown to science. Many of these may even be
susceptible to disappearance before their formal
description. Recent efforts from environmental
sequencing and cultivation approaches have
revealed the existence and ecological roles of several novel algal lineages distributed across the
eukaryotic tree of life (Not et al. 2007, Moore et al.
2008, Lepère et al. 2009, Liu et al. 2009, Shi et al.
2009). The study published by Ichinomiya et al. in
this issue is a convincing example of how the inventory of algal diversity could be fundamental for our
understanding of the evolution of life.
The Parmales are small (2–5 lm) spherical microalgae covered by siliceous plates that sometimes
bear astonishing spinelike projections (Booth and
Marchant 1987, Kosman et al. 1993). The Parmales
were originally thought to be resting stages of
loricate choanoflagellates (Silver et al. 1980). However, discovery of a functional chloroplast led to
their classification within the Heterokontophyta
(Marchant and McEldowney 1986). They have been
tentatively included in the Chrysophyceae since
their formal description by Booth and Marchant in
1987, but in the absence of cultures, this proposition has been debated for decades. Ichinomiya et al.
demonstrate that rather than being chrysophytes,
the Parmales are in fact a sister group of the
diatoms and are intimately associated with (and
probably synonymous to) another recently described
algal class, the Bolidophyceae (Guillou et al. 1999a).
This discovery is highly significant because diatoms have been one of the most abundant and
productive (and hence biogeochemically active)
lineages of photosynthetic eukaryotes on Earth
since the Mesozoic era (Falkowski et al. 2004), but
their origin is rather obscure. This discovery is also
unexpected because to date the Bolidophyceae are
exclusively comprised of small (<3 lm) naked
biflagellates devoid of siliceous ornamentation
(Guillou et al. 1999a). Are the Parmales and the
Bolidomonadales two distinct ploidy stages within
the same heteromorphic haplo-diplontic life cycle?
And how could this discovery help us to better
understand the emergence of diatoms?
The origin of diatoms has long been discussed in
the literature (Round 1981, Mann and Marchant
1989, Medlin et al. 1997, Sims et al. 2006). Diatoms
are easily distinguished from other microalgae due
to their silicified cell walls (frustules) composed of
two overlapping rigid valves and girdle bands. Diatoms are unusual among unicellular organisms in
having a truly diplontic life cycle, with no mitosis
occurring during the haploid phase. Round and
Crawford (1981) were the first to propose that diatoms arose from an ancestor covered by siliceous
scales that differentiated into the two valves and the
girdle bands observed in modern diatoms. However,
Mann and Marchant (1989) were the first to link
this transformation to the life cycle of the ancestor
of diatoms. They hypothesized that diatoms evolved
from a diploid zygotic siliceous stage of an originally
haplontic prediatom with a flagellate vegetative
phase. This theory is in part supported by the production of small, naked uniflagellate haploid
gametes during sexual reproduction of some basal
centric diatoms. The study of Ichinomiya et al. published in this issue brings an important new piece to
the puzzle. Diatoms may actually have evolved from
the diploid stage of an organism with truly haplodiplontic life cycle.
This concept assumes of course that the ancestor
of diatoms resembles the Parmales ⁄ Bolidophyceae,
and that the siliceous Parmales are diploid while
the naked Bolidomonas are haploid. The Parmales
sequence provided by Ichinomiya et al. has >99%
sequence similarity with that of Bolidomonas pacifica.
Although more evidence is needed to prove that a
real haplo-diplontic life cycle occurs between both
taxa, this hypothesis should be easier to test now
with the availability of cultures.
More generally, this discovery emphasizes the
importance of sex in microalgae (recently review by
2
ALGAE HIGHLIGHTS
3
*
FIG. 1. Worldwide distribution of Bolidophyceae and Parmales. In black: Environmental sequences from marine ecosystems; in gray
(with exterior line in black): environmental sequences from a freshwater lake; in red: Bolidomonas-like strains deposited in the Roscoff Culture Collection (RCC; http://www.sb-roscoff.fr/Phyto/RCC/); in blue: observation of Parmales by microscopy; in white (with exterior line
in blue): strain isolated by Ichinomiya et al. from this issue. *Observation made from sample collected at 2,800 m depth.
Von Dassow and Montresor 2011) and the probable
underestimation of the occurrence of haplo-diplontic lifestyles. The haplo-diplontic life cycle is widespread in eukaryotes, occurring notably in
macroalgae (red, green, and brown), Haptophyta,
some fungi, Foraminifera, mosses, and ferns. It
involves obligate cycling between independent, freeliving haploid and diploid phases, both capable of
mitosis. The persistence of haplo-diplontic life cycles
is still not well understood but may have several
advantages (Valero et al. 1992, Jenkins 1993,
Richerd et al. 1993, Mable and Otto 1998, Thornber
2006). Genetically, if the life-cycle phases have equal
duration, then the cost of sex in monophasic cycles
(haplontic or diplontic) is twice that in a biphasic
cycle (Richerd et al. 1993). Additionally, as asexual
proliferations occur during both phases, two different dispersal modes are possible in biphasic life
cycles (Mable and Otto 1998). Haplo-diplontic life
cycles may also have ecological advantages when
each phase has different physiological requirements
(and sometimes completely different phenotypes),
increasing de facto the potential for a species to
occupy a broader range of environmental niches
(Hughes and Otto 1999). During antagonistic interactions, heteromorphic life histories may help to
resist strong grazing pressure (Lubchenco and Cubit
1980) and parasites (Frada et al. 2008).
Little is known about the biogeographic distribution and ecology of either the Bolidophyceae or the
Parmales. Screening of a database containing
>130,000 eukaryotic SSU rDNA sequences allowed
the detection of 86 environmental sequences closely
associated to known Bolidophyceae sequences
(Fig. 1). These sequences derive from samples taken
from equatorial to polar waters, leading to the conclusion that the Parmales ⁄ Bolidomonadales are
widely distributed in marine waters. Additionally, the
recent detection of Bolidophyceae-like sequences
from a freshwater lake (Richards et al. 2005) highlighted their eventual capacity to colonize continental ecosystems as well. This last point may be
highly significant for paleontology, given that the
oldest recorded fossil diatoms were from nonmarine
sediments from 175 million years ago (Harwood
et al. 2004).
From direct observations, the Parmales have regularly been reported in polar waters (Fig. 1) at concentrations of >105 cells Æ L)1 during the productive
season (Booth et al. 1980, Buck and Garrison 1983).
They were also reported in relatively high abundance in productive warmer waters off the Mexican
coast (Bravo-Sierra and Hernández-Becerril 2003).
Parmales-like materials are commonly reported in
fecal pellets, leading to the conclusion that they are
heavily grazed by larger predators (Kosman et al.
1993). By contrast, Bolidophyceae culture strains
have predominantly been obtained from oligotrophic waters (Fig. 1) where they have been
reported at relatively low concentrations (Guillou
et al. 1999b, Not et al. 2005). As a lot of microalgae,
they are suspected to be mixotrophic and recently
stressed as one of the most important grazers of the
two oceanic cyanobacteria prey Prochlorococcus and
Synechococcus (Frias-Lopez et al. 2009).
From these observations, one can suspect that
Bolidomonas-like organisms are ecologically important
in oceanic and oligotrophic waters while Parmales
are more frequently reported from more coastal
and rich waters. This difference might be correlated
4
A L G A E H I G H L I G H TS
to the theory that there is a strong selection for
smaller cell sizes (with higher surface area to volume ratio) in oligotrophic waters, which likely favor
the smallest haploid stages (Lewis 1985). How global change will affect this distribution and eventually the putative life cycle of the Parmales ⁄
Bolidophyceae is an open question.
LAURE GUILLOU
CNRS ⁄ UPMC, UMR 7144,
Adaptation et Diversité en Milieu Marin,
Station Biologique de Roscoff,
Place Georges Teissier, 29680 Roscoff, France
[email protected]
Booth, B. C., Lewin, J. & Norris, R. E. 1980. Siliceous nanoplankton
I. Newly discovered cysts from the Gulf of Alaska. Mar. Biol.
58:205–9.
Booth, B. C. & Marchant, H. J. 1987. Parmales, a new order of
marine chrysophytes, with descriptions of three new genera
and seven new species. J. Phycol. 23:245–60.
Bravo-Sierra, E. & Hernández-Becerril, D. U. 2003. Parmales
(Chrysophyceae) from the Gulf of Tehuantepec, Mexico,
including the description of a new species, Tetraparma insecta
sp. nov., and a proposal to the taxonomy of the group.
J. Phycol. 39:577–83.
Buck, K. R. & Garrison, D. L. 1983. Protists from the ice-edge
region of the Weddell Sea. Deep-Sea Res. 30:1261–77.
Falkowski, P. G., Katz, M. E., Knoll, A. H., Quigg, A., Raven, J. A.,
Schofield, O. & Taylor, F. J. R. 2004. The evolution of modern
eukaryotic phytoplankton. Science 305:354–60.
Frada, M., Probert, I., Allen, M. J., Wilson, W. H. & de Vargas, C.
2008. The ‘‘Cheshire Cat’’ escape strategy of the coccolithophore Emiliania huxleyi in response to viral infection. Proc. Natl.
Acad. Sci. U. S. A. 105:15944–9.
Frias-Lopez, J., Thompson, A., Waldbauer, J. & Chisholm, S. W.
2009. Use of stable isotope-labelled cells to identify active
grazers of picocyanobacteria in ocean surface waters. Environ.
Microbiol. 11:512–25.
Guillou, L., Chrétiennot-Dinet, M. J., Medlin, L. K., Claustre, H.,
Loiseaux-de-Goër, S. & Vaulot, D. 1999a. Bolidomonas: a new
genus with two species belonging to a new algal class, the
Bolidophyceae (Heterokonta). J. Phycol. 35:368–81.
Guillou, L., Moon-van der Staay, S. Y., Claustre, H., Partensky, F. &
Vaulot, D. 1999b. Diversity and abundance of Bolidophyceae
(Heterokonta) in two oceanic regions. Appl. Environ. Microbiol.
65:4528–36.
Harwood, D. M., Chang, K. H. & Nikolaev, V. A. 2004. Late Jurrassic
to earliest Cretaceous diatoms from Jasong Synthem, Southern
Korea: evidence for a terrestrial origin. In Witkowski, A.,
Radziejewska, T., Wawrzyniak-Wydrowska, B., DaniszewskaKowalczyk, G. & Bak, M. [Eds.] 18th International Diatom
Symposium, Miedzyzdroje, Poland, p. 81.
Hughes, J. S. & Otto, S. P. 1999. Ecology and the evolution of
biphasic life cycles. Am. Nat. 154:306–20.
Jenkins, C. D. 1993. Selection and the evolution of genetic life
cycles. Genetics 133:401–10.
Kosman, C. A., Thomsen, H. A. & Østergaard, J. B. 1993. Parmales
(Chrysophyceae) from Mexican, Californian, Baltic, Arctic and
Antarctic waters with the description of a new subspecies and
several new forms. Phycologia 32:116–28.
Lepère, C., Vaulot, D. & Scanlan, D. J. 2009. Photosynthetic picoeukaryote community structure in the South East Pacific
Ocean encompassing the most oligotrophic waters on Earth.
Environ. Microbiol. 11:3105–17.
Lewis, W. M., Jr. 1985. Nutrient scarcity as an evolutionary cause of
haploidy. Am. Nat. 125:692–701.
Liu, H., Probert, I., Uitz, J., Claustre, H., Aris-Brosou, S., Frada, M.,
Not, F. & de Vargas, C. 2009. Extreme diversity in noncalcifying haptophytes explains a major pigment paradox in open
oceans. Proc. Natl. Acad. Sci. U. S. A. 106:12803–8.
Lubchenco, J. & Cubit, J. 1980. Heteromorphic life histories of
certain marine algae as adaptations to variations in herbivory.
Ecology 61:676–87.
Mable, B. K. & Otto, S. P. 1998. The evolution of life cycles with
haploid and diploid phases. Bioessays 20:453–62.
Mann, D. G. & Marchant, H. J. 1989. The origins of the diatom and
its life cycle. In Green, J. C., Leadbeater, B. S. C. & Diver, W. I.
[Eds.] The Chromophyte Algae: Problems and Perspectives. Clarendon Press, Oxford, UK, pp. 307–23.
Marchant, H. J. & McEldowney, A. 1986. Nanoplankton siliceous
cysts from Antarctica are algae. Mar. Biol. 92:53–7.
Medlin, L. K., Kooistra, W. H. C. F., Gersonde, R., Sims, P. A. &
Wellbrock, U. 1997. Is the origin of the diatoms related to the
end-Permian mass extinction? Nova Hedwigia 65:1–11.
Moore, R. B., Obornı́k, M., Janouškovec, J., Chrudimsky, T., Vancová,
M., Green, D. H., Wright, S. W., et al. 2008. A photosynthetic
alveolate closely related to apicomplexan parasites. Nature
451:959–63.
Not, F., Massana, R., Latasa, M., Marie, D., Colson, C., Eikrem, W.,
Pedrós-Alió, C., Vaulot, D. & Simon, N. 2005. Late summer
community composition and abundance of photosynthetic
picoeukaryotes in Norwegian and Barents Seas. Limnol. Oceanogr. 50:1677–86.
Not, F., Valentin, K., Romari, K., Lovejoy, C., Massana, R., Töbe, K.,
Vaulot, D. & Medlin, L. 2007. Picobiliphytes: a marine picoplanktonic algal group with unknown affinities to other
eukaryotes. Science 315:252–4.
Richards, T. A., Vepritskiy, A. A., Gouliamova, D. E. & NierzwickiBauer, S. A. 2005. The molecular diversity of freshwater
picoeukaryotes from an oligotrophic lake reveals diverse, distinctive and globally dispersed lineages. Environ. Microbiol.
7:1413–25.
Richerd, S., Couvet, D. & Valéro, M. 1993. Evolution of the alternance of haploid and diploid phases in life cycles. II. Maintenance of the haplo-diplontic cycle. J. Evol. Biol. 6:263–80.
Round, F. E. 1981. Some aspects of the origin of diatoms and their
subsequent evolution. Biosystems 14:483–6.
Round, F. E. & Crawford, R. M. 1981. The lines of evolution of the
Bacillariophyta. I. Origin. Proc. R. Soc. Lond. B 211:237–60.
Shi, X. L., Marie, D., Jardillier, L., Scanlan, D. J. & Vaulot, D. 2009.
Groups without cultured representatives dominate eukaryotic
picophytoplankton in the oligotrophic South East Pacific
Ocean. PLoS ONE 4:e7657.
Silver, M. W., Mitchell, J. G. & Ringo, D. L. 1980. Siliceous
nanoplankton. II. Newly discovered cysts and abundant choanoflagellates from the Weddell Sea, Antarctica. Mar. Biol.
58:211–7.
Sims, P. A., Mann, D. G. & Medlin, L. K. 2006. Evolution of the
diatoms: insights from fossil, biological and molecular data.
Phycologia 45:361–402.
Thornber, C. S. 2006. Functional properties of the isomorphic
biphasic algal life cycle. Integr. Comp. Biol., doi: 10.1093/icb/
icl018.
Valero, M., Richerd, S., Perrot, V. & Destombe, C. 1992. Evolution
of alternation of haploid and diploid phases in life cycles.
Trends Ecol. Evol. 7:25–9.
Von Dassow, P. & Montresor, M. 2011. Unveiling the mysteries of
phytoplankton life cycles: patterns and opportunities behind
complexity. J. Plankton Res. 33:3–12.