Photosynthetic picoplankton or picophytoplankton is the fraction of the

phytoplankton Phytoplankton () are the autotrophic (self-feeding) components of the plankton community and a key part of ocean and freshwater ecosystems. The name comes from the Greek words (), meaning 'plant', and (), meaning 'wanderer' or 'drifter'. ...

performing

photosynthesis Photosynthesis is a process used by plants and other organisms to convert light energy into chemical energy that, through cellular respiration, can later be released to fuel the organism's activities. Some of this chemical energy is stored in ...

composed of

cells Cell most often refers to: * Cell (biology), the functional basic unit of life Cell may also refer to: Locations * Monastic cell, a small room, hut, or cave in which a religious recluse lives, alternatively the small precursor of a monastery w ...

between 0.2 and 2 µm in size ( picoplankton). It is especially important in the central

oligotroph An oligotroph is an organism that can live in an environment that offers very low levels of nutrients. They may be contrasted with copiotrophs, which prefer nutritionally rich environments. Oligotrophs are characterized by slow growth, low rates o ...

ic regions of the world oceans that have very low concentration of

nutrients A nutrient is a substance used by an organism to survive, grow, and reproduce. The requirement for dietary nutrient intake applies to animals, plants, fungi, and protists. Nutrients can be incorporated into cells for metabolic purposes or excr ...

History

* 1952: Description of the first truly picoplanktonic species, ''Chromulina pusilla'', by Butcher.Butcher, R. (1952). Contributions to our knowledge of the smaller marine algae. ''Journal of the Marine Biological Association of the UK'' 31: 175-91. This species was renamed in 1960 to '' Micromonas pusilla''Manton, I. & Parke, M. (1960). Further observations on small green flagellates with special reference to possible relatives of ''Chromulina pusilla'' Butcher. ''Journal of the Marine Biological Association of the UK'' 39: 275-98. and a few studies have found it to be abundant in temperate oceanic waters, although very little such quantification data exists for eukaryotic picophytoplankton. * 1979: Discovery of marine ''

Synechococcus ''Synechococcus'' (from the Greek ''synechos'', in succession, and the Greek ''kokkos'', granule) is a unicellular cyanobacterium that is very widespread in the marine environment. Its size varies from 0.8 to 1.5 µm. The photosynthetic c ...

'' by WaterburyWaterbury, J. B. ''et al.'' (1979). Wide-spread occurrence of a unicellular, marine planktonic, cyanobacterium. ''Nature'' 277: 293-4. and confirmation with electron microscopy by Johnson and Sieburth.Johnson, P. W. & Sieburth, J. M. (1979). Chroococcoid cyanobacteria in the sea: a ubiquitous and diverse phototrophic biomass. ''Limnology and Oceanography'' 24: 928-35. * 1982: The same Johnson and Sieburth demonstrate the importance of small eukaryotes by electron microscopy.Johnson, P. W. & Sieburth, J. M. (1982). In-situ morphology and occurrence of eucaryotic phototrophs of bacterial size in the picoplankton of estuarine and oceanic waters. ''Journal of Phycology'' 18: 318-27. * 1983: W.K.W Li and colleagues, including

Trevor Platt Trevor Charles Platt (August 12, 1942 - April 6, 2020) was a British and Canadian biological oceanographer who was distinguished for his fundamental contributions to quantifying primary production by phytoplankton at various scales of space an ...

show that a large fraction of marine primary production is due to organisms smaller than 2 µm.Li, W. K. W. ''et al.'' (1983). Autotrophic picoplankton in the tropical ocean. ''Science'' 219: 292-5. * 1986: Discovery of "prochlorophytes" by Chisholm and Olson in the Sargasso Sea,Chisholm, S. W. ''et al.'' (1988). A novel free-living prochlorophyte occurs at high cell concentrations in the oceanic euphotic zone. ''Nature'' 334: 340-3. named in 1992 as ''

Prochlorococcus ''Prochlorococcus'' is a genus of very small (0.6 μm) marine cyanobacteria with an unusual pigmentation ( chlorophyll ''a2'' and ''b2''). These bacteria belong to the photosynthetic picoplankton and are probably the most abundant photosynth ...

marinus''.Chisholm, S. W. ''et al.'' (1992). ''Prochlorococcus marinus'' nov. gen. nov. sp.: an oxyphototrophic marine prokaryote containing divinyl chlorophyll ''a'' and ''b''. ''Archives of Microbiology'' 157: 297-300. * 1994: Discovery in the Thau lagoon in France of the smallest photosynthetic eukaryote known to date, '' Ostreococcus tauri'', by Courties.Courties, C. ''et al.'' (1994). Smallest eukaryotic organism. ''Nature'' 370: 255. * 2001: Through sequencing of the

ribosomal RNA Ribosomal ribonucleic acid (rRNA) is a type of non-coding RNA which is the primary component of ribosomes, essential to all cells. rRNA is a ribozyme which carries out protein synthesis in ribosomes. Ribosomal RNA is transcribed from riboso ...

gene extracted from marine samples, several European teams discover that eukaryotic picoplankton are highly diverse.López-García, P. ''et al.'' (2001). Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. ''Nature'' 409: 603-7.Moon-van der Staay, S. Y. ''et al.'' (2001). Oceanic 18S rDNA sequences from picoplankton reveal unsuspected eukaryotic diversity. ''Nature'' 409: 607-10. This finding followed on the first discovery of such eukaryotic diversity in 1998 by Rappe and colleagues at Oregon State University, who were the first to apply rRNA sequencing to eukaryotic plankton in the open-ocean, where they discovered sequences that seemed distant from known phytoplanktonRappe, M. ''et al.'' (1998). Phylogenetic diversity of ultraplankton plastid Small-Subunit rRNA genes recovered in environmental nucleic acid samples from the Pacific and Atlantic coasts of the United States. ''Applied and Environmental Microbiology'' 64294-303. The cells containing DNA matching one of these novel sequences were recently visualized and further analyzed using specific probes and found to be broadly distributed.Kim, E., Harrison, J., Sudek, S. ''et al.'' (2011). Newly identified and diverse plastid-bearing branch on the eukaryotic tree of life. Proceedings of the National Academy of Sciences USA. Vol. 108: 1496-1500.

Methods of study

Because of its very small size, picoplankton is difficult to study by classic methods such as optical microscopy. More sophisticated methods are needed. *

Epifluorescence microscopy A fluorescence microscope is an optical microscope that uses fluorescence instead of, or in addition to, scattering, reflection, and attenuation or absorption, to study the properties of organic or inorganic substances. "Fluorescence microsc ...

allows researchers to detect certain groups of cells possessing

fluorescent Fluorescence is the emission of light by a substance that has absorbed light or other electromagnetic radiation. It is a form of luminescence. In most cases, the emitted light has a longer wavelength, and therefore a lower photon energy, ...

pigments such as ''

'' which possess

phycoerythrin Phycoerythrin (PE) is a red protein-pigment complex from the light-harvesting phycobiliprotein family, present in cyanobacteria, red algae and cryptophytes, accessory to the main chlorophyll pigments responsible for photosynthesis.The red pigment ...

. *

Flow cytometry Flow cytometry (FC) is a technique used to detect and measure physical and chemical characteristics of a population of cells or particles. In this process, a sample containing cells or particles is suspended in a fluid and injected into the flow ...

measures the size (" forward scatter ") and fluorescence of 1,000 in 10,000 cells per second. It allows one to determine very easily the concentration of the various picoplankton populations on marine samples. Three groups of cells (''

'', ''

'' and picoeukaryotes) can be distinguished. For example ''Synechococcus'' is characterized by the double fluorescence of its pigments: orange for phycoerythrin and red for

chlorophyll Chlorophyll (also chlorophyl) is any of several related green pigments found in cyanobacteria and in the chloroplasts of algae and plants. Its name is derived from the Greek words , ("pale green") and , ("leaf"). Chlorophyll allow plants to ...

. Flow cytometry also allows researchers to sort out specific populations (for example ''Synechococcus'') in order put them in culture, or to make more detailed analyses. * Analysis of photosynthetic

pigments A pigment is a colored material that is completely or nearly insoluble in water. In contrast, dyes are typically soluble, at least at some stage in their use. Generally dyes are often organic compounds whereas pigments are often inorganic compoun ...

such as chlorophyll or

carotenoids Carotenoids (), also called tetraterpenoids, are yellow, orange, and red organic pigments that are produced by plants and algae, as well as several bacteria, and fungi. Carotenoids give the characteristic color to pumpkins, carrots, parsnips, co ...

by high precision chromatography (

HPLC High-performance liquid chromatography (HPLC), formerly referred to as high-pressure liquid chromatography, is a technique in analytical chemistry used to separate, identify, and quantify each component in a mixture. It relies on pumps to p ...

) allows researchers to determine the various groups of algae present in a sample. * Molecular biology techniques: :*

Cloning Cloning is the process of producing individual organisms with identical or virtually identical DNA, either by natural or artificial means. In nature, some organisms produce clones through asexual reproduction. In the field of biotechnology, c ...

and

sequencing In genetics and biochemistry, sequencing means to determine the primary structure (sometimes incorrectly called the primary sequence) of an unbranched biopolymer. Sequencing results in a symbolic linear depiction known as a sequence which suc ...

genes In biology, the word gene (from , ; "...Wilhelm Johannsen coined the word gene to describe the Mendelian units of heredity..." meaning ''generation'' or ''birth'' or ''gender'') can have several different meanings. The Mendelian gene is a ba ...

such as that of

, which allows researchers to determine total diversity within a sample :* DGGE (Denaturing Gel Electrophoresis), that is faster than the previous approach allows researchers to have an idea of the global diversity within a sample :* In situ hybridization (

FISH Fish are Aquatic animal, aquatic, craniate, gill-bearing animals that lack Limb (anatomy), limbs with Digit (anatomy), digits. Included in this definition are the living hagfish, lampreys, and Chondrichthyes, cartilaginous and bony fish as we ...

) uses fluorescent probes recognizing specific

taxon In biology, a taxon ( back-formation from '' taxonomy''; plural taxa) is a group of one or more populations of an organism or organisms seen by taxonomists to form a unit. Although neither is required, a taxon is usually known by a particular n ...

, for example a

species In biology, a species is the basic unit of classification and a taxonomic rank of an organism, as well as a unit of biodiversity. A species is often defined as the largest group of organisms in which any two individuals of the appropriat ...

, a

genus Genus ( plural genera ) is a taxonomic rank used in the biological classification of living and fossil organisms as well as viruses. In the hierarchy of biological classification, genus comes above species and below family. In binomial nom ...

or a

class Class or The Class may refer to: Common uses not otherwise categorized * Class (biology), a taxonomic rank * Class (knowledge representation), a collection of individuals or objects * Class (philosophy), an analytical concept used differently ...

.Not, F. ''et al.'' (2004). A single species ''Micromonas pusilla'' (Prasinophyceae) dominates the eukaryotic picoplankton in the western English Channel. ''Applied and Environmental Microbiology'' 70: 4064-72. This original description as a species is now thought to be composed of a number of different

cryptic species In biology, a species complex is a group of closely related organisms that are so similar in appearance and other features that the boundaries between them are often unclear. The taxa in the complex may be able to hybridize readily with each ot ...

, a finding that has been confirmed by a genome sequencing project of two strains led by researchers at the

Monterey Bay Aquarium Research Institute The Monterey Bay Aquarium Research Institute (MBARI) is a private, non-profit oceanographic research center in Moss Landing, California. MBARI was founded in 1987 by David Packard, and is primarily funded by the David and Lucile Packard Founda ...

.Worden, A.Z., ''et al.'' (2009). Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes ''Micromonas''. ''Science'' 324: 268-272. :* Quantitative PCR can be used, as FISH, to determine, the abundance of specific groups. It has the main advantage to allow the rapid analysis of a large number of samples simultaneously,Johnson, Z. I. ''et al.'' (2006). Niche partitioning among ''Prochlorococcus'' ecotypes along ocean-scale environmental gradients. ''Science'' 311: 1737-40. but requires more sophisticated controls and calibrations.

Composition

Three major groups of organisms constitute photosynthetic picoplankton: *

Cyanobacteria Cyanobacteria (), also known as Cyanophyta, are a phylum of gram-negative bacteria that obtain energy via photosynthesis. The name ''cyanobacteria'' refers to their color (), which similarly forms the basis of cyanobacteria's common name, bl ...

belonging to the genus ''

'' of a size of 1 µm (micrometer) were first discovered in 1979 by J. Waterbury (

Woods Hole Oceanographic Institution The Woods Hole Oceanographic Institution (WHOI, acronym pronounced ) is a private, nonprofit research and higher education facility dedicated to the study of marine science and engineering. Established in 1930 in Woods Hole, Massachusetts, i ...

). They are quite ubiquitous, but most abundant in relatively mesotrophic waters. * Cyanobacteria belonging to the genus ''

'' are particularly remarkable. With a typical size of 0.6 µm, ''Prochlorococcus'' was discovered only in 1988 by two American researchers, Sallie W. (Penny) Chisholm (

Massachusetts Institute of Technology The Massachusetts Institute of Technology (MIT) is a private land-grant research university in Cambridge, Massachusetts. Established in 1861, MIT has played a key role in the development of modern technology and science, and is one of th ...

) and R.J. Olson (

). In spite of its small size, this photosynthetic organism is undoubtedly the most abundant of the planet: indeed its density can reach up to 100 million cells per liter and it can be found down to a depth of 150 m in all the intertropical belt.Partensky, F. ''et al.'' (1999). ''Prochlorococcus'', a marine photosynthetic prokaryote of global significance. ''Microbiology and Molecular Biology Reviews'' 63: 106-27. * Picoplanktonic

eukaryotes Eukaryotes () are organisms whose cells have a nucleus. All animals, plants, fungi, and many unicellular organisms, are Eukaryotes. They belong to the group of organisms Eukaryota or Eukarya, which is one of the three domains of life. Bacter ...

are the least well known, as demonstrated by the recent discovery of major groups. Andersen created in 1993 a new

of brown algae, the

Pelagophyceae Pelagophycidae is a sub class of heterokont algae.It is the sister group of the axodines. Together, they form the class Dictyochophyceae. All known species are marine. They can be single-celled ( coccoid or flagellate A flagellate is a c ...

.Andersen, R. A. ''et al.'' (1993). Ultrastructure and 18S rRNA gene sequence for '' Pelagomonas calceolata'' gen. and sp. nov. and the description of a new algal class, the Pelagophyceae classis nov. ''Journal of Phycology'' 29: 701-15. More surprising still, the discovery in 1994 of a eukaryote of very small size, '' Ostreococcus tauri'', dominating the phytoplanktonic biomass of a French brackish lagoon (étang de Thau), shows that these organisms can also play a major ecological role in coastal environments. In 1999, yet a new class of alga was discovered,Guillou, L. ''et al.'' (1999). ''Bolidomonas'': a new genus with two species belonging to a new algal class, the Bolidophyceae (Heterokonta). ''Journal of Phycology'' 35: 368-81. the

Bolidophyceae Bolidophyceae is a class of photosynthetic heterokont picophytoplankton, and consist of less than 20 known species. They are distinguished by the angle of flagellar insertion and swimming patterns as well as recent molecular analyses. Bolidophyc ...

, very close genetically of

diatoms A diatom (Neo-Latin ''diatoma''), "a cutting through, a severance", from el, διάτομος, diátomos, "cut in half, divided equally" from el, διατέμνω, diatémno, "to cut in twain". is any member of a large group comprising sev ...

, but quite different morphologically. At the present time, about 50 species are known belonging to several classes. ::: The use of molecular approaches implemented since the 1990s for bacteria, were applied to the photosynthetic picoeukaryotes only 10 years later around 2000. They revealed a very wide diversity and brought to light the importance of the following groups in the picoplankton : * Prasinophyceae *

Haptophyta The haptophytes, classified either as the Haptophyta, Haptophytina or Prymnesiophyta (named for '' Prymnesium''), are a clade of algae. The names Haptophyceae or Prymnesiophyceae are sometimes used instead. This ending implies classification at ...

Cryptophyta The cryptophyceae are a class of algae, most of which have plastids. About 220 species are known, and they are common in freshwater, and also occur in marine and brackish habitats. Each cell is around 10–50 μm in size and flattened in shape ...

In temperate coastal environment, the genus '' Micromonas'' (Prasinophyceae) seems dominant. However, in numerous oceanic environments, the dominant species of eukaryotic picoplankton remain still unknown.Worden, A.Z. & Not, F.(2008) Ecology and Diversity of Picoeukaryotes. Book Chapter in: Microbial Ecology of the Ocean, 2nd Edition. Ed. D. Kirchman. Wiley.

Ecology

Each picoplanktonic population occupies a specific

ecological niche In ecology, a niche is the match of a species to a specific environmental condition. Three variants of ecological niche are described by It describes how an organism or population responds to the distribution of resources and competitors (for ...

in the oceanic environment. * The ''

'' cyanobacterium is generally abundant in mesotrophic environments, such as near the equatorial

upwelling Upwelling is an physical oceanography, oceanographic phenomenon that involves wind-driven motion of dense, cooler, and usually nutrient-rich water from deep water towards the ocean surface. It replaces the warmer and usually nutrient-depleted ...

or in coastal regions. * The ''

'' cyanobacterium replaces it when the waters becomes impoverished in nutrients (i.e.,

ic). On the other hand, in temperate regions such as the North Atlantic Ocean, ''Prochlorococcus'' is absent because the cold waters prevent its development. * The diversity of eukaryotes derives from their presence in a large variety of environments. In oceanic regions, they are often observed at depth, at the base of the well-lit layer (the "euphotic" layer). In coastal regions, certain sorts of picoeukaryotes such as '' Micromonas'' dominate. As with larger plankton, their abundance follows a seasonal cycle with a maximum in summer. Thirty years ago, it was hypothesized that the speed of division for micro-organisms in central oceanic ecosystems was very slow, of the order of one week or one month per generation. This hypothesis was supported by the fact that the

biomass Biomass is plant-based material used as a fuel for heat or electricity production. It can be in the form of wood, wood residues, energy crops, agricultural residues, and waste from industry, farms, and households. Some people use the terms bio ...

(estimated for example by the contents of

) was very stable over time. However, with the discovery of the picoplankton, it was found that the system was much more dynamic than previously thought. In particular, small

predator Predation is a biological interaction where one organism, the predator, kills and eats another organism, its prey. It is one of a family of common feeding behaviours that includes parasitism and micropredation (which usually do not kill t ...

s of a size of a few micrometres which ingest picoplanktonic algae as quickly as they were produced were found to be ubiquitous. This extremely sophisticated predator-prey system is nearly always at equilibrium and results in a quasi-constant picoplankton biomass. This close equivalence between production and consumption makes it extremely difficult to measure precisely the speed at which the system turns over. In 1988, two American researchers, Carpenter and Chang, suggested estimating the speed of cell division of phytoplankton by following the course of

DNA replication In molecular biology, DNA replication is the biological process of producing two identical replicas of DNA from one original DNA molecule. DNA replication occurs in all living organisms acting as the most essential part for biological inheritan ...

by microscopy. By replacing the microscope by a

flow cytometer Flow cytometry (FC) is a technique used to detect and measure physical and chemical characteristics of a population of cells or particles. In this process, a sample containing cells or particles is suspended in a fluid and injected into the flow ...

, it is possible to follow the DNA content of picoplankton cells over time. This allowed researchers to establish that picoplankton cells are highly synchronous: they replicate their DNA and then divide all at the same time at the end of the day. This synchronization could be due to the presence of an internal biological clock.

Genomics

In the 2000s,

genomics Genomics is an interdisciplinary field of biology focusing on the structure, function, evolution, mapping, and editing of genomes. A genome is an organism's complete set of DNA, including all of its genes as well as its hierarchical, three-dim ...

allowed to cross a supplementary stage. Genomics consists in determining the complete sequence of

genome In the fields of molecular biology and genetics, a genome is all the genetic information of an organism. It consists of nucleotide sequences of DNA (or RNA in RNA viruses). The nuclear genome includes protein-coding genes and non-coding ...

of an organism and to list every

gene In biology, the word gene (from , ; "...Wilhelm Johannsen coined the word gene to describe the Mendelian units of heredity..." meaning ''generation'' or ''birth'' or ''gender'') can have several different meanings. The Mendelian gene is a b ...

present. It is then possible to get an idea of the metabolic capacities of the targeted organisms and understand how it adapts to its environment. To date, the genomes of several types of ''

''Rocap, G. ''et al.'' (2003). Genome divergence in two ''Prochlorococcus'' ecotypes reflects oceanic niche differentiation. ''Nature'' 424: 1042-7.Dufresne, A. ''et al.'' (2003). Genome sequence of the cyanobacterium ''Prochlorococcus marinus'' SS120, a nearly minimal oxyphototrophic genome. ''Proceedings of the National Academy of Sciences of the United States of America'' 100: 10020-5. and ''

'',Palenik, B. ''et al.'' (2003). The genome of a motile marine ''Synechococcus''. ''Nature'' 424: 1037-42. and of a strain of '' Ostreococcus''Derelle, E. ''et al.'' (2006). Genome analysis of the smallest free-living eukaryote ''Ostreococcus tauri'' unveils many unique features. ''Proceedings of the National Academy of Sciences of the United States of America'' 103: 11647-52. have been determined. The complete genomes of two different Micromonas strains revealed that they were quite different (different species) - and had similarities with land plants. Several other cyanobacteria and of small eukaryotes (''Bathycoccus'', ''Pelagomonas'') are under sequencing. In parallel, genome analyses begin to be done directly from oceanic samples (ecogenomics or métagenomics),Venter, J. C. ''et al.'' (2004). Environmental genome shotgun sequencing of the Sargasso Sea. ''Science'' 304: 66-74. allowing us to access to large sets of gene for uncultivated organisms. :::

Notes and references

Bibliography

;Cyanobacteria * Zehr, J. P., Waterbury, J. B., Turner, P. J., Montoya, J. P., Omoregie, E., Steward, G. F., Hansen, A. & Karl, D. M. 2001. Unicellular cyanobacteria fix N2 in the subtropical North Pacific Ocean. Nature 412:635-8 ;Eukaryotes * Butcher, R. 1952. Contributions to our knowledge of the smaller marine algae. J. Mar. Biol. Assoc. UK. 31:175-91. * Manton, I. & Parke, M. 1960. Further observations on small green flagellates with special reference to possible relatives of Chromulina pusilla Butcher. J. Mar. Biol. Assoc. UK. 39:275-98. * Eikrem, W., Throndsen, J. 1990. The ultrastructure of ''Bathycoccus'' gen. nov. and ''B. prasinos'' sp. nov., a non-motile picoplanktonic alga (Chlorophyta, Prasinophyceae) from the Mediterranean and Atlantic. Phycologia 29:344-350 * Chrétiennot-Dinet, M. J., Courties, C., Vaquer, A., Neveux, J., Claustre, H., ''et al.'' 1995. A new marine picoeucaryote: ''Ostreococcus tauri'' gen et sp nov (Chlorophyta, Prasinophyceae). Phycologia 34:285-292 * Sieburth, J. M., M. D. Keller, P. W. Johnson, and S. M. Myklestad. 1999. Widespread occurrence of the oceanic ultraplankter, ''Prasinococcus capsulatus'' (Prasinophyceae), the diagnostic "Golgi-decapore complex" and the newly described polysaccharide "capsulan". J. Phycol. 35: 1032-1043. * Not, F., Valentin, K., Romari, K., Lovejoy, C., Massana, R., Töbe, K., Vaulot, D. & Medlin, L. K. 2007. Picobiliphytes, a new marine picoplanktonic algal group with unknown affinities to other eukaryotes. Science 315:252-4. * Vaulot, D., Eikrem, W., Viprey, M. & Moreau, H. 2008. The diversity of small eukaryotic phytoplankton (≤3 μm) in marine ecosystems. FEMS Microbiol. Rev. 32:795-820. ;Ecology * Platt, T., Subba-Rao, D. V. & Irwin, B. 1983. Photosynthesis of picoplankton in the oligotrophic ocean. Nature 300:701-4. * Stomp M, Huisman J, de Jongh F, Veraart AJ, Gerla D, Rijkeboer M, Ibelings BW, Wollenzien UIA, Stal LJ. 2004. Adaptive divergence in pigment composition promotes phytoplankton biodiversity. Nature 432: 104-107. * Campbell, L., Nolla, H. A. & Vaulot, D. 1994. The importance of ''Prochlorococcus'' to community structure in the central North Pacific Ocean. Limnol. Oceanogr. 39:954-61. ;Molecular Biology and Genomes * Rappé, M. S., P. F. Kemp, and S. J. Giovannoni. 1995. Chromophyte plastid 16S ribosomal RNA genes found in a clone library from Atlantic Ocean seawater. J. Phycol. 31: 979-988. {{plankton Biological oceanography Planktology Aquatic ecology Cyanobacteria Algae