Overview

Brief Summary

Cafeteria roenbergensis is a single-celled flagellate from marine environments. It is D-shaped, and about 5-10 µm and has a volume of about 20 µm 3(where 1 µm, a micron, is one-thousandth of a millimeter). It is a eukaryotic organism, with a nucleus, mitochondria and other subcellular compartments. The posterior flagellum attaches the organism to the substrate while it is feeding. If it detaches, the cell will swim around being pulled forward by the beating of the anterior flagellum. When feeding, the action of the anterior flagellum creates a current of water that moves towards the cell. The current carries bacteria, and these are the primary food of the flagellate. The food is ingested below the base of the flagella – this is referred to as the ventral side. The flagella are anchored by ‘rootlets’ ribbons and subcellular ropes. They act as a skeleton and also support the mouth region. Cafeteria roenbergensis was the first species in the genus to be described, and was described only in 1988. It, like many other smaller members of the ocean communities, had largely been overlooked until the 1980s. At that time, it became increasingly evident that bacteria and the organisms that eat them play a very major role in moving food, nutrients and energy in marine ecosystems. As ocean environments are the only environments in which there is a net burial of carbon, a number of major research projects emerged in the1980s to improve our understanding of marine ecosystems typically within the context of global climate change. Cafeteria roenbergensis occurs in all oceans in which they have been looked for, and can grow to very high concentrations (in excess of 10,000 per ml). They are weeds, growing rapidly when food is available and under a reasonably wide range of conditions. It is usually assumed that this species serves as food for larger protozoa or small invertebrate animals, but recent work suggests that the populations are also ‘controlled’ by viruses. Because they are easy to grow, Cafeteria roenbergensis has been subject to a diversity of more detailed studies, such as genomic and ecological studies. From these studies come useful gems such that the mitochondria of all eukaryotes studied, this species have the most functionally compact DNA – with only 3.4% not being used for coding purposes (Hauth et al. 2005).

The name Cafeteria reflects the importance of this organism in marine microbial food webs.

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Small (less than 1/100 millimeter) marine flagellate found in oceans world-wide, eats bacteria.
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Comprehensive Description

Description of Cafeteria roenbergensis

Cells are D-shaped, 2 to 5 microns long, and laterally compressed. There is a shallow groove on the left side of the cell. Two flagella of similar length emerge subapically and are slightly longer than the cell. The anterior (= feeding = hairy - the hairs are not visible by light microscopy) flagellum is directed perpendicular to the ventral face of the cell of attached cells. The posterior flagellum is reflexed, passing over one face of the cell and then attaching to the substrate by the tip. In swimming cells, the anterior flagellum is directed forwards and beats with a sine-wave, and the posterior flagellum is directed backwards and trails. Usually the cells move quickly following a spiral path, but sometimes they move slowly. Bacteria may be ingested near the anterior part or posterior part of the ventral groove. Acronema sippiwissettensis Teal et al.,1998 cannot be readily distinguished from this species, nor can Cafeteria mylnikovi at a structural level, but is said to differ in sequence characteristics of the small ribosomal RNA molecule.
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biopedia

Source: BioPedia

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“Etymology’ is a term used by nomenclaturalists to explain how the name of a taxon was derived. There are an array of codes of nomenclature (such as those for Animals, plants and fungi, bacteria and Archaea, fossils, cultivated plants, viruses, and for phylogeneticists) that regulate the way names can be formed. The rules for giving names for plants, animals, fungi, and prokaryotes (viruses excepted) are largely similar. Typically, a species name will have two parts, first the genus name and then be followed by the name of the species. The Genus and species name are written in italics, with the Genus name capitalized. Often, this binomial will be followed by the names of the people who first created the name (the authority information).

The binomial convention dates from Linnaeus in the 18th century as an abbreviation of a longer and more descriptive piece of text. The names are written as if in Latin, and rules of classical (Latin and Greek) grammar typically apply. Many taxonomists will try to find Latin or Greek words that refer to some distinctive feature of the organism, or they will name a taxon after a person or a place. The species name, ‘roenbergensis’ refers to the fact that it was first recognized from water samples taken near the Danish village of Rønbjerg.

As for Cafeteria, this has a more whimsical derivation. This species was described as the concept of ‘microbial food webs’ was becoming established. This concept recognized that a very large proportion of nutrient and energy turnover in the oceans was being mediated by the microbial community and not by the larger and more familiar organisms. Those organisms that ate bacteria and similarly sized eukaryotic algae were emerging as the principal consumers within the oceans. The key players turned out to be small flagellated protozoa. The authors were struggling to find a name that reflected the ecological significance of the organisms, and just as they were giving one evening, the hostelry along the road from the Rønbjerg marine station switched on its lights, and provided the inspiration for this name.

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Distribution

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MICROBIS

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The genus Cafeteria has been known for less than 20 years and data on distribution is limited. It has been reported from marine, hypersaline and brackish environments from around the world. We believe that the morphospecies probably has a world-wide distribution, following the concept that for microbial species ‘everything is everywhere’ and represented in all ecosystems in which it tolerates prevailing physical and chemical conditions.

As yet, we have only a very poor understanding of its ecological preferences, its biochemistry or physiology. A truly remarkable state of affairs for an organism that is very significant in its own right and as a representative of a major category of microbial consumers.

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Physical Description

Cells of Cafeteria roenbergensis are D-shaped, 2-5 microns long, with two flagella emerging near the apex, or tip of cell. In non-swimming cells, the posterior flagellum passes over one face of the cell and attaches to the substrate. In swimming cells, the anterior flagellum is directed forwards and beats to propel the cell in a spiral-like motion, while the posterior flagellum trails behind. The cells have one nucleus and five mitochondria, and like other stramenpiles the cristae is tubular. There is a shallow groove on the left side of the cell, through which bacteria may be ingested anteriorly or posteriorly. Pseudobodo tremulans's cells are slightly larger, 4.5-6 microns long, with an anterior "collar" or lip-like structure around the anterior end of the cell. There are two flagella which behave much like that of Cafeteria roenbergensis. Bicosoecid cells are heterotrophic, and reproduce only through asexual binary division; no other reproductive method has been found.

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MicrobeWiki

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Uninucleate trophic cells are approximately bean-shaped and only 3-10 µm long. The two flagella are subapically inserted, often from a conspicuous pocket over which hangs a liplike protrusion. The anterior flagellum is usually directed forward, the posterior flagellum backward. Sessile cells rest on the tip of the posterior flagellum, with the anterior flagellum beating in a helicoidal fashion and directing a current of water onto the cell body. This behavior is diagnostic for bicosoecids.
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Protist Image Data

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Cafeteria is a genus of small marine flagellates – a type of protozoon. Like other flagellates, they are just one cell, with a nucleus, and feed or move using undulating flagella. Cafeteria has two flagella, one that attaches to the substrate in feeding cells, the other (anterior) undulates actively to draw food to the cell. In unattached cells, the anterior flagellum projects in front of the cell to draw it forward. Cafeteria roenbergensis was the first species described in the genus. Some comments on other species are included in the section on ‘Taxonomy and evolution’. Cells are typically D-shaped, the flat side of the ‘D’ being referred to as ventral, with the flagella inserting at the anterior end of the ventral side. The anterior flagellum is the feeding / swimming flagellum, and it has stiff hairs on it. These have the effect of reversing the thrust of the flagellum so that while it beats from base to tip, water is pulled towards the cell or the cell moves with the flagellum pointing forwards. The more posteriorly inserting flagellum seems to have a sticky tip and it adheres to the substrate. Both flagella are usually a little longer than the cell, though can vary in length by a factor of about 2.

We often understand the detailed architecture inside the flagellates that have been described in the last 20 years or so. This 'ultrastructural identity' is put together from analyses of electron micrographs. The information that is produced, especially in relation to the anchorage of the flagella, is often of great help in understanding the relationships of the species to other organisms.

Cafeteria has two flagella that give rise to four microtubular roots. This is usual in most stramenopiles (see section on Taxonomy and evolution).

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Morphology

Description of rootlets

Stramenopiles typically have four microtubular roots arising from a pair of basal bodies (kinetosomes). This drawing shows the basal bodies of the two flagella (two is the hairy one) and the (blue) microtubular rootlets associated with the flagella. These serve to anchor the basal bodies as the flagella beat along with other materials such as the grey linkages to the basal bodies and the rhizostyle. Also they arc round the cytostome (mouth) to give it support. The arrangement of these rootlets is resolved by cutting several series of thin sections through individual cells, and then reconstructing the entire organization from the sections. The rootlets help systematists in resolving relationships among protist taxa.

References

O'Kelly C. J. and D. J. Patterson. 1996. The flagellar apparatus of Cafeteria roenbergensis Fenchel & Patterson, 1988 (Bicosoecales = Bicosoecida). European Journal of Protistology 32: 216-226.

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Diagnostic Description

Genus Cafeteria Fenchel and Patterson 1988. Biflagellated suspension feeding protists without chloroplasts, without lorica. Two flagella insert subapically on ventral side. Feeding cells are attached to the substrate with the posterior tip of the recurrent flagellum. The anterior flagellum extends laterally; it carries tubular hairs. Detached cells swim with the recurrent flagellum trailing behind the cell and the anterior flagellum pointing forward. A naked bicosoecid. One species known.

Species C. Roenbergensis Fenchel and Patterson 1988. Cafeteria measuring 4 6 µm in length, with flat unembellished ventral surface. From marine habitats.

Other species: Cafeteria marsupialis, Cafeteria minima, Cafeteria mylnikovii

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Cells are 2 – 10 µm long, D-shaped and laterally compressed, with a shallow groove on the left side. Two flagella emerge subapically and are slightly longer than the cell. Cells often attach to the substrate by the tip of the posterior flagellum, which is held in a curve. In attached cells the anterior flagellum is directed laterally. In swimming cells, the anterior flagellum is directed anteriorly and beats with a sine wave, while the posterior flagellum trails. Food particles are ingested near the posterior part of the ventral groove. Cells were observed in both sediment and mat samples.

Fenchel, T. and D. J. Patterson. 1988. Cafeteria roenbergensis nov. gen., nov. sp., a heterotrophic microflagellate from marine plankton. Marine Microbial Food Webs 3: 9-19.

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Type Information

Type locality: Denmark: Limfjord
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Ecology

Habitat

Depth range based on 1 specimen in 1 taxon.

Environmental ranges
  Depth range (m): 0.75 - 0.75
 
Note: this information has not been validated. Check this *note*. Your feedback is most welcome.

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General Ecology

Cafeteria roenbergensis uses its anterior, hairy, flagellum to create a current of water that draws food particles to the body. Particles around 1 micron in diameter - such as bacteria, cyanobacteria and bacterial-sized eukaryotes – are actively ingested. According to Boenigk and Arndt 2000, the flagella beat about 40 times per second, and they create a water current that moves about 100 microns / second. This allows them to filter about 0.002 nl / individual / second. As flagellates may be present in concentrations in excess of 1000 per ml, a dense population can filter all of the water around them in less than half an hour. When a bacterium is drawn to the ventral surface of the body, the beat pattern of the flagellum changes to help rotate the bacterium so it lies parallel to the long axis, before it is ingested at the cytostome region on the ventral surface. If bacteria are abundant, fifteen bacteria may be consumed per cell per hour. Unless the bacterium is too large, in which case it is rejected, the ingested bacterium is segregated within a food vacuole, which then moves into the cell body for digestion, and the flagellum begins normal beating again.

When bacterivorous flagellates are compared, Cafeteria is distinctive because it needs relatively high concentrations of bacteria. In addition, when offered bacteria and beads, other species eject the beads more quickly after ingesting them. Overall, Cafeteria roenbergensis, is more like a gourmand than a gourmet.

Cells can replicate in under 10 hours. They reproduce by binary fission, first replicating the flagella and internal organelles before the cell divides. No sexual activity is known for this species.

The fate of Cafeteria roenbergensis after growth is not known. No cysts have been reported for this species. In some cases, they can be infected by viruses and this can cause the collapse of populations (Massana et al., 2007). We may assume that they are consumed by protozoa such as tintinnids that filter particles about 5 µm in diameter, or by small metazoa.

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Cafeteria roenbergensis is a good ‘model’ for bacterivorous flagellates (HNF = heterotrophic nanoflagellates) of the marine microbial food web.

The microbial food web refers to the interactions of microbial species in ecosystems. Most descriptions of marine ecosystems focus on a carbon and energy flow that begins with larger phytoplankton such as diatoms and dinoflagellates, and track the passage through layers of consumption via crustacea, fish to the larger consumers. In the 1980's, it became clear that this pathway probably accounted for less than 5% of the carbon flow. The primary producers themselves are very leaky and a high proportion of the carbon produced by photosynthesis diffuses out the cells where it can be captured by bacteria. Every transaction in the food chain is inefficient, such that up to 90% of the carbon / energy in the transaction may be returned to the environment where it is available for smaller organisms – again including bacteria. Bacteria are benefit from the deaths of larger organisms, or from the collapse of algal blooms. Much of the debris settles to the ocean floor as ‘marine snow’ where it nourishes microbial communities.

Also, diatoms and dinoflagellates are not the only producers in the oceans. Vents that release heated (or cold) water and dissolved inorganics are an energy source for benthic communities which form complex communities that can include worms and molluscs. In the upper layers of water in which sunlight penetrates, many smaller algae add to the primary production. Especially in deeper waters, cyanobacteria and bacterial-sized eukaryotes (picoplankton) make very significant contributions to overall carbon fixation.

Overall bacteria and bacteria-sized eukaryotes are very significant primary producers or secondary producers that consume dissolved and particulate carbon material. In turn these are resources for larger consumers or for viruses. The HNF, such as Cafeteria roenbergensis, are the primary consumers of this microbial production. Cafeteria seems to be less efficient than related species, but is a weed and grows well when food is relatively abundant.

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Evolution and Systematics

Systematics or Phylogenetics

Molecular Phylogeny

Fucus distichusHeterosigma akashiwoCytosiphon lomentariaCostaria costataSynura sphagnicolaMallomonas rasilisOchromonas distigmaThalassiosira pseudonanaThalassiosira weissflogiiLabyrinthulidsOomycetesdiatomsbrown algaeSchizochytrium minutumSchizochytrium mangroveiAplanochytrium kerguliensisAplanochytrium stocchinoiThraustochytrium aggregatumJaponochytrium marinumSchizochytrium aggregatumCaecitellus parvulusCafateria roenbergensisAchlya bisexualisLeptoglena chapmaniiApodachlya brachynemaPhytophthora palmivoraLagenidium giganteumAureococcus anophagefferensPelagomonas calceolataPseudonitzschia multiseriesNitzschia thermalisPhaeodactylum tricornutumSkeletonema costatum

Figure legend: This diagram shows the similarity of the same gene in Cafeteria roenbergensis and a number of other stramenopile species. The bases that make up the gene are subject to cumulative change over time, such that when comparisons are made, those which are similar and more likely to be closely related can be identified. In this 'tree', Cafeteria is found near the base, among groups that are all heterotrophs (oomycete fungi, labyrinthulids, Caecitellus). All of the species with chloroplasts, Aureococcus and above in this diagram, form a branch, suggesting that the stramenopiles were originally colourless heterotrophs and late acquired chloroplasts. Image provided by Jessica Grant and the EUTREE ATOL project

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Higher level affiliations

Up one level – the genus Cafeteria

Fenchel and Patterson in describing the genus in 1988 referred to biflagellated protists without chloroplasts or a lorica, but used one of the two flagella to create a current of water from which they picked out suspended particles.  Feeding cells attach to the substrate with the posterior tip of the recurrent flagellum while detached cells swim with the recurrent flagellum trailing behind the cell and the anterior flagellum pointing forward.  So far only described from marine environments.  It was originally described with just Cafeteria roenbergensis in the genus. Since that time several additional species have been added. 

Cafeteria marsupialis was described by Larsen and Patterson in 1990, is a slightly larger species than C. roenbergensis (from 5- 15 microns long) but with a generally similar aspect.   Food is ingested at the posterior end of the ventral side and an ingestion region is usually quite visible.  The species tends to occur in organically enriched and slightly anoxic environments.

Cafeteria minuta is the smallest species in the genus, it was first described by Jakoba Ruinen as a species of Pseudobodo.  The body is typically less than 5 microns long, but the anterior flagellum is over 10 microns long.  This species is rarely reported.

Cafeteria ligulifera is also a small species (5 microns of less in length), but has a distinctive shelf extending from the ventral face of the body, and both flagella are significantly longer than the length of the body.  This species is rarely reported.

Cafeteria mylnikovii Cavalier-Smith and Chao closely resembles Cafeteria roenbergensis in size and shape.  It is said to differ because the anterior flagellum can have a longer maximal length.  There are differences in composition of the 18S rRNA of a Norwegian strain of C. roenbergensis and the strain described as C. mylnikovi – and it is said that there is a distinctive 18S rDNA signature at nucleotide positions 1278-1294.

Species concepts among heterotrophic flagellates generally and Cafeteria species in particular have not been much discussed.   Especially given the absence of sexual reproduction and the size and extent of the global population, species will show some variation.  We can therefore expect to encounter morphological and molecular variation as well as ecological preferences within each ‘entity’.  How we draw lines between 'species' remains unclear, and it is possible that the morphological and molecular variations reported below as discriminating species may eventually be regarded as intraspecific variation.

The genus Acronema was created by Teal et al. (Teal et al. 1998), which, at the light microscopical level, is held to differ from Cafeteria because it has flagella that are narrower at their tips than elsewhere in the flagellum (i.e. are acronematic).  However, images of Cafeteria marsupialis and Cafeteria ligulifera in Larsen and Patterson (1990) show that the tip of the posterior flagellum is narrower than the rest of the flagellum, i.e. is acronematic.  It is likely that further study will reveal that this species is in fact a species of Cafeteria, and probably Cafeteria roenbergensis.

Bicosoecids – the next level up

Heterotrophic flagellates that can adhere by the tip of the recurrent flagellum and feed by drawing water towards the cell by the action of the anterior hairy flagellum are typically assigned to the bicosoecids (some times referred to as bicoecids).  The best known genus with about 40 species is Bicosoeca, which is distinctive because the cells live within organic loricas.  One species has loricas interconnected to form a colony structure.

One other common non-loricate genus is Pseudobodo.  Normally, it does not stick directly to the substrate with the flagellum, but by a thin strand of mucus arising from the tip of the shorter recurrent flagellum.  This genus has a raised collar around the front part of the cell.  Marine, common, and cosmopolitan.

There are an array of other heterotrophic flagellates which, like the bicosoecids, lie near the base of the stramenopile tree (see below), but precise relationships have yet to be clarified.  There are two genera with a single flagellum (Anoeca Cavalier-Smith and Chao, 2006) and Siluania Karpov et al 1998, and several biflagellated genera that do not attach by the tip of the posterior flagellum.  They include, Developayella Tong, 1995; Pendulomonas Tong, 1997, Wobblia Moriya et al 2000, and Placidia Morya et al. 2002.
A slightly more unusual form is Commation Thomsen and Larsen, 1993, a gliding circular or ovoid flattened cell  with a proboscis.  There is a single hairy flagellum that emerges at the base of the proboscis.  It glides by a process that seems to involce the secretion of mucus. 

Next step up - Caecitellus and pseudodendromonads

As we progress away from the taxa that are filter feeders, we encounter the genera Caecitellus, Pseudodendromonas, Adriomonas, and Cyathobodo.  The latter three are pseudodendromonads. All of these taxa have flagella without stuiff hairs, and have a well developed arc of microtubules surrounding an ingestion region where bacteria are consumed.  As all four genera  lack hairs on the flagella, and as these hairs define the stramenopiles, these flagellates may either be the sister group to the stramenopiles (i.e. branched off prior to the original of the tripartite hairs) or are an early lineage within the starmenpiles that secondarily lost flagellar hairs.

Stramenopiles

The stramenopiles are a major group of protists to which Cafeteria belongs.  The group is defined by the stiff 3-part hairs that attach to the flagellum.  All stramenopiles have these hairs or have evolved from organisms with these. Some stramenopiles (e.g. opalines) have secondarily lost the hairs and even the flagella (actinophryids and diatoms).

The effect of the hairs is to reverse the thrust of the beating flagellum, such that water is drawn towards the cell despite the flagellar beat progressing from base to tip.  This is shown in the animation in the media panel above.

Electron-micrograph of a part of the anterior flagellum of the stramenopile Paraphysomonas butcheri showing the flagellar hairs (mastigonemes). There are three parts to the hairs, a basal flexible section, a long stiff tube that ends in a small number of flimsy hairs.  The flagellum is about half a micron in diameter.  Image by N. Voers.

The Stramenopiles are diverse.  The group includes some very large organisms (such as brown seaweeds), some very speciose (many species) groups such as the diatoms, some endosymbionts (such as the opalines), fungus-like oomycetes that include the organisms that caused the Irish potato famine, many algae (also referred to as heterokonts) and a variety of heterotrophic organisms. Some of the heterotrophic (without plastids that carry out photosynthesis) stramenopiles lost their plastids secondarily (as in the pedinellids and actinophryid heliozoa), but most appear to be among the very early evolving stramenopiles.  This suggests that this lineage evolved from heterotrophic organisms.

Most stramenopiles have chloroplasts. They include brown algae and diatoms. The group of eukaryotes that are most closely related to the stramenopiles (the sister group) is not known.  One prevalent idea is that the stramenopiles are related to other organisms with similar brownish chloroplasts (haptophytes and cryptophytes) – collectively refrerred to as the chromists.  Most molecular studies into evolutionary relationship fail to confirm this hypothesis, such that it seems likely that the chromists are polyphyletic (come from different immediate ancestors) and that the early stramenopiles were not chromists but heterotrophs like Cafeteria or its close relatives.

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Molecular Biology and Genetics

Molecular Biology

Barcode data: Cafeteria roenbergensis

The following is a representative barcode sequence, the centroid of all available sequences for this species.


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© Barcode of Life Data Systems

Source: Barcode of Life Data Systems (BOLD)

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Statistics of barcoding coverage: Cafeteria roenbergensis

Barcode of Life Data Systems (BOLDS) Stats
Public Records: 1
Specimens with Barcodes: 1
Species With Barcodes: 1
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© Barcode of Life Data Systems

Source: Barcode of Life Data Systems (BOLD)

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Mitochondrial Genome

Pink is Adenine, Green is Cytosine, Yellow is Thymine and Blue is Guanine (Reads upper-left to lower-right).

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Wikipedia

Cafeteria roenbergensis

Cafeteria roenbergensis is a marine Bicosoecid described in 1988 by Fenchel and D.J. Patterson. It is the first known species of Cafeteria.

Contents

Description

Cafeteria roenbergensis is D-shaped and has a volume of around 20 µm3. Being a eukaryotic organism it has a nucleus, mitochondria and other subcellular compartments. The posterior flagellum attaches the organism to the substrate while it is feeding. If it detaches, the cell will swim around being pulled forward by the beating of the anterior flagellum. When feeding, the action of the flagellum creates a current of water that moves towards the cell. The current carries bacteria - the primary food of the flagellate. The food is ingested below the base of the flagella – this is referred to as the ventral side. The flagella are anchored by ‘rootlets’ ribbons and subcellular ropes. They act as a skeleton and also support the mouth region.

Cells can replicate in under 10 hours. They reproduce by binary fission, first replicating the flagella and internal organelles before the cell divides. No sexual activity is known for this species.

The flagella beat about 40 times per second, and they create a water current that moves about 100 micrometres / second.

Ecology

Cafeteria roenbergensis occurs in all oceans in which they have been looked for, and can grow to very high concentrations (in excess of 10,000 per ml). They may be the most abundant predator on the planet.[1]

Genome

Of all eukaryotes studied, this species has the most functionally compact mitochondrial DNA – with only 3.4% not being used for coding purposes.

Name

Marine biologist Tom Fenchel, one of the two species authorities who first described C. roenbergensis, is credited with having joked about the chromalveolate's name:

"We found a new species of ciliate during a marine field course in Rønbjerg and named it Cafeteria roenbergensis because of its voracious and indiscriminate appetite after many dinner discussions in the local cafeteria."
—Tom Fenchel[2]

The Marine Ecology Research Station at Rønbjerg at the Limfjord in Denmark belongs to Århus University.[3]

Virus

The giant virus Cafeteria roenbergensis virus (CroV) lives within C. roenbergensis organisms.[4]

References

  1. ^ Baldauf, S.L. (2008). "An overview of the phylogeny and diversity of eukaryotes". Journal of Systematics and Evolution 46 (3): 263–273. doi:10.3724/SP.J.1002.2008.08060 (inactive 2009-03-13). http://www.plantsystematics.com/qikan/manage/wenzhang/jse08060.pdf. 
  2. ^ Fenchel, T. (November 1988). "Marine Plankton Food Chains". Annual Review of Ecology and Systematics 19 (1): 19–38. doi:10.1146/annurev.es.19.110188.000315. http://arjournals.annualreviews.org/doi/abs/10.1146/annurev.es.19.110188.000315?prevSearch=%255Bauthor%253A%2Bfenchel%255D&searchHistoryKey=. Retrieved 20 September 2009. 
  3. ^ Rønbjerg, Department of Biological Sciences, Århus University]
  4. ^ Fischer, M. G.; Allen, M. J.; Wilson, W. H.; Suttle, C. A. (2010). "Giant virus with a remarkable complement of genes infects marine zooplankton". Proceedings of the National Academy of Sciences 107 (45): 19508–19513. Bibcode 2010PNAS..10719508F. doi:10.1073/pnas.1007615107.  edit

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References and More Information

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