We have an innate desire to pigeonhole life which is largely due to our ability to communicate in various ways, thereby necessitating a system that ensures we can define what it is we are referring to. An inevitable outcome of defining an item is giving it a name. In biology, taxonomy sets out the rules defining what makes something unique, while nomenclature applies a set of rules or codes for naming. For plant life, this delineation started with Carl Linnaeus’ Species Plantarum of 1753. To this day the fundamental principles of Linnaeus remain—a specimen is selected as the basis for the description, this being referred to as the ‘type’ specimen. Any individual considered to match this description is considered to be a member of the species. Linnaean genus and species names together with names for other ranks (such as family, class, etc.) can and should serve to express a great many viewpoints as to relationships between taxa, i.e. systematics.

Fig. 1. Light micrographs of Isochrysis galbana (left) and Tisochrysis lutea (formerly Isochrysis aff. galbana or T-iso). Scale bar = 5 um

The taxonomy and systematics of microalgae have historically been based almost exclusively on comparison of morphological criteria. Nowadays, microalgal systematics is greatly influenced by data derived from DNA extracted from nuclei, mitochondria and chloroplasts, leading to the discovery of many cryptic species that demonstrate a decoupling between morphological conservatism and genetic variability. On balance, it is our opinion that molecularbased systematics should now be considered more of an exact science than the traditional morphological based taxonomy, but there is as yet no consensus on how to integrate this new knowledge in the most informative yet practical manner into the Linnaean nomenclatural system. Here we outline a few recent examples that illustrate this important issue in different ways.

A haptophyte culture strain assigned to Isochrysis affinis galbana (Tahiti isolate, commonly known as ‘T-Iso’) is widely used in aquaculture due to its exceptional lipid content and thus high nutritional value. Despite seemingly being morphologically identical to type material of Isochrysis galbana, comparison of conservative (slowly evolving) genetic markers has demonstrated that T-Iso is clearly genetically distinct from this taxon (Figure 1), with the genetic distance being equivalent to that commonly found between different genera within the haptophytes. It has therefore been classified in a new genus, Tisochrysis, as a new species, T. lutea. The creation of a new genus based on genetic data reflects the fact that this is a fairly extreme example of cryptic species, but the practical consequence is that the Linnaean names no longer convey unique information on morphology and any organism identified by microscopy as fitting the morphological description cannot be assigned to one or other of the species without DNA sequencing.

Fig. 2. Light micrographs of the ventral view of Karenia mikimotoi isolated from three geographical locations: United Kingdom (A), Japan (B) and New Zealand (C). Scale bar = 10 um.

There are numerous examples of less extreme, but nonetheless significant genetic diversity occurring within morphospecies. Karenia mikimotoi (Figure 2) is a widespread toxic HAB dinoflagellate taxon, but morphometric plasticity within clonal isolates and between specimens assigned to this species (or to Gymnodinium nagasakiense or Gyrodinium aureolum, two species generally regarded as conspecific with K. mikimotoi) has caused notorious taxonomic confusion. In 2011 Manal Al-Kandari and colleagues at the Marine Biological Association applied a combination of nuclear and chloroplast gene markers to positively discriminate between isolates collected from Europe, New Zealand and Japan. Whilst isolates from all of these geographical localities exhibited similar morphologies (Figure 2), genetic evidence indicates distinct cladistic features. The European and New Zealand isolates have more in common with each other than the Japanese isolates, and only the Japanese isolates were shown to produce harmful toxins Gymnocin A & B+. Al-Kandari chose to distinguish the two genetic clades that they identified within K. mikimotoi as sub-species, termed K. mikimotoi mikimotoi and K. mikimotoi aureolum. In other cases where significant intramorphospecies genetic diversity has been discovered, terms such as ‘clade’ (for the dinoflagellate Symbiodinium microadriaticum or the prasinophyte Micromonas pusilla, for example) or ‘ecotype’ (for the cyanobacterium Synechococcus) have been used. Use of an epithet such as ‘clade’ with a Linnaean name has the advantage of conveying information on both morphological similarity and genetic differentiation of cryptic taxa, but does not provide a clear idea of the investigator’s opinion of where species boundaries lie.

In fact, this might actually be considered an advantage in light of the large-scale genomic information that is becoming increasingly available. A key member of the haptophytes is the iconic calcifying coccolithophore Emiliania huxleyi that is classified in a separate genus from another very common coccolithophore, Gephyrocapsa oceanica, due to a highly visible, but structurally extremely minor difference in the form of the calcite crystals making up the calcite scales (coccoliths) that cover the cells (Figure 3). Emiliania huxleyi is a very young morphospecies in evolutionary terms, palaeontological evidence suggesting a recent divergence from G. oceanica around 291 thousand years ago. Genetic studies indicate that they are very closely related species that should at least be classified in the same genus. Despite its recent emergence, significant genetic diversity has been detected within E. huxleyi using both mitochondrial and a nuclear-encoded marker, this diversity corresponding to either biogeography or minor morphological variations in the degree of calcification of coccoliths, respectively. The full genome sequence of one strain of E. huxleyi and large-scale sequence data from 13 other strains have recently been published and these data reveal that members of the E. huxleyi morphospecies exhibit a ‘pan genome’: reflecting extensive genome variability (as much as 25% variability in gene content between different E. huxleyi strains) and different metabolic repertoires. Gephyrocapsa oceanica, as well as other Gephyrocapsa species, are likely genetic variants of the E. huxleyi pan genome. The taxonomic implications of such observations are not yet clear, but it seems evident that as the genomic era progresses, our current quest to pigeonhole biological entities into species will be seriously challenged.

Fig. 3. Typical morphologies of Gephyrocapsa oceanica (left) and Emiliania huxleyi. They can be clearly distinguished by the resolution of scanning electron microscopy (top panel); while under light microscopy they are indistinctive. Scale bar = 1 um.

We might do well to attempt to devise and code a nomenclatural system that focuses on conveying a much broader range of standardized and complementary information than at present; without necessarily having the pretention of ringfencing (and typifying) species, and potentially with more emphasis on describing strains and shared features between strains, such as pan genomes. Linnaean names could obviously be an integral part of such a system, for example if there is general agreement that their use should be restricted to conveying morphological information only. These examples add to the ever-growing body of evidence of molecular schemes challenging morphological assumptions in many different ways. But alas, change does not come easy. Taxonomic changes impact the nomenclature of well-known organisms that is often deeply entrenched in academic and societal usage, a factor that tends to lead to resistance to the adoption of new descriptions and names (let alone a new nomenclatural system). Nonetheless, taxonomy is a classification science and therefore by its very nature is subject to evolutionary processes based on advances in the state of knowledge about groups of organisms. Carefully defined names are and will remain a powerful means to convey the state-of-the-art of this knowledge.

El-Mahdi Bendif1 (elmben@ mba.ac.uk), Manal Al-Kandari2 , Ian Probert3 and Declan C Schroeder1 (dsch@mba.ac.uk)

1. The Marine Biological Association

2. Kuwait Institute for Scientific Research

3. UPMC/CNRS Station Biologique de Roscoff

GLOSSARY

Microalgae Microscopic unicellular photosynthetic life forms.

Morphospecies Species that are morphologically almost identical but genetically different.

HAB Species that cause Harmful Algal Blooms.

Plasticity Morphological variability related to changing environment.

Coccolithophore From greek: coccos or kokkos= berry, lithos= stones, i.e., cells covered by calcium carbonate.

Pan genome a set of core genes plus genes distributed variably between strains.

FURTHER READING

Al-Kandari M., Highfield A., Hall M., Hayes P. & Schroeder, D.C. 2011. Molecular tools separate Harmful Algal Bloom species, Karenia mikimotoi, from different geographical regions into distinct sub-groups. Harmful Algae doi:10.1016/j.hal.2011.04.017

Bendif E.M., Probert I., Schroeder D.C. & de Vargas C. 2013a. On the description of Tisochrysis lutea gen. nov. sp. nov. and Isochrysis nuda sp. nov. in the Isochrysidales, and the transfer of Dicrateria to the Prymnesiales ( Haptophyta ). Journal of Applied Phycology (in press):10.1007/s10811-013-0037-0

Bendif E.M., Probert I., Carmichael C., Romac S., Hagino K. & de Vargas C. 2013b Genetic delineation between and within the world plankton morpho-species Emiliania huxleyi and Gephyrocapsa oceanica (Haptophyta, coccolithophores). Journal of Phycology. (in review)

Hagino K., Bendif E.M., Young J., Kogame, K., Takano, Y., Probert, I., Horiguchi, T., de Vargas, C. & Okada, H. 2011. New evidence for morphological and genetic variation in the cosmopolitan coccolithophore Emiliana huxleyi (Prymnesiophyceae) from the cox1b-ATP4 genes. Journal of Phycology 47:1164-1176 -

Read B. A., Kegel J., Klute M. J., Kuo A., Lefebvre S. C., Maumus F., Mayer C., Miller J., Monier A., Salamov A., Aguilar M., Claverie J-M., Frickenhaus S., Gonzalez K., Herman E.K., Lin Y-C., Napier J., Ogata H.i, Sarno A. F., Shmutz J., Schroeder D., de Vargas C., Verret F., von Dassow P., Valentin K., Van de Peer Y., Wheeler G., Emiliania huxleyi Annotation Consortium, Dacks J. B.,. Delwiche C. F, Dyhrman S. T., Glöckner G., John U., Richards T., Worden A. Z., Young J., Zhang X. & Grigoriev I. V. 2013 Emiliania’s pan genome drives the phytoplankton’s global distribution. Nature doi:10.1038/nature12221

Schroeder D.C., Biggi G. F., Hall M., Davy J., Martinez Martinez J., Richardson A., Malin G. & Wilson W.H. (2005) A genetic marker to separate Emiliania huxleyi (Prymnesiophyceae) morphology. Journal of Phycology. 41: 874-879.

Author

El-Mahdi Bendif and colleagues.

Category