PhycologyCourse handouts

EuglenidsKalle Olli1

AbstractEuglenids are a group of >1500 described species of single-celled flagellates with diverse modes of nutrition, includingphagotrophy and photoautotrophy.Almost all euglenids are free-living. The (usually) one or two emergent flagella have thick paraxonemal (paraxial)rods and originate in a deep pocket/reservoir, while the cell surface is almost always supported by a pellicle of parallelproteinaceous strips underlain by microtubules.Cells with 4–12 strips are rigid; most of those with more strips (typically ca 20–40) have them arranged helically andexhibit active cell deformation called euglenid motion or metaboly.Most phagotrophic euglenids are surface-associated bacterivores or eukaryovores that employ a flagellar gliding motility.They are abundant in marine and freshwater sediments.Photoautotrophic species (Euglenophyceae) constitute a single subclade within euglenids and have a plastid(chloroplast) of secondary endosymbiotic origin, with three bounding membranes. The plastid is typically green,with chlorophylls a + b, and was derived from a green alga related to the Pyramimonadales. Photoautotrophiceuglenids move primarily by swimming, and most (members of the taxon Euglenales, e.g., Euglena) have a singleemergent flagellum and are generally restricted to fresh and brackish waters.

1EMU

Contents

Introduction 1Where do euglenids belong? . . . . . . . . . . . . . 2Nutritional diversity . . . . . . . . . . . . . . . . . . 2Euglenids are ambiregnal . . . . . . . . . . . . . . . 4Practical importance . . . . . . . . . . . . . . . . . . 4

Characteristic features in a nutshell 4

Pellicle and metaboly 5

Cell structures 6Flagella and locomotion . . . . . . . . . . . . . . . . 6

Paraxonemal rods . . . . . . . . . . . . . . . . 6Flagella hair . . . . . . . . . . . . . . . . . . . 6Gliding . . . . . . . . . . . . . . . . . . . . . 6Swimming . . . . . . . . . . . . . . . . . . . . 6

Feeding apparatus . . . . . . . . . . . . . . . . . . . 6Plastids . . . . . . . . . . . . . . . . . . . . . . . . 8Photoreception . . . . . . . . . . . . . . . . . . . . 9Mitochondrion . . . . . . . . . . . . . . . . . . . . . 9

Habitats 9

Euglenophyte examples 10Trachelomonas . . . . . . . . . . . . . . . . . . . .10Colacium . . . . . . . . . . . . . . . . . . . . . . .11Phacus . . . . . . . . . . . . . . . . . . . . . . . . .11Euglena . . . . . . . . . . . . . . . . . . . . . . . .11Eutreptiella . . . . . . . . . . . . . . . . . . . . . .12

Acknowledgments 12

References 12

Introduction

Euglenids (syn. euglenoids) are a prominent group of free-living, aquatic flagellates, usually with one or two activeflagella. Most of the >1500 descibed species are unicellsthat are 5–50 μm in length, a few are larger.

Almost all are motile. There are three types of motion:

• Swimming• Surface-associated gliding• Euglenid motion or metaboly

Figure 1. Scanning electron micrographs showing the diversity of euglenids. (a) Petalomonad (phagotroph), (b) Ploeotiid (phagotroph),(c) Euglena (phototroph), (d) Monomorphina (phototroph), (e) Phacus (phototroph). (f–g) Lepocinclis (phototroph). Images not to scale;all cells between 10 and 100 μm. Source: [Leander et al.(2017)Leander, Lax, Karnkowska, and Simpson]

Where do euglenids belong?Euglenids, along with Kinetoplastea (all heterotrophic) be-long to Euglenozoa, which is one of the major sub-groupsof eucaryotes.The common features of Euglenozoa include:

• The flagella are inserted at the base of a deep pocket (alsoknown as the reservoir).

• Active flagella are conspicuously thickened due to thepresence of paraxonemal rods.

• The mitochondrial cristae are also discoidal.

Distinguishing feature of euglenids — their cell surfacearchitecture is almost always supported by a pellicle of abut-ting parallel strips of protein that lie directly under the cellmembrane (Fig. 1). Cells with many helically arrangedstrips (>20) are often capable of a characteristic squirmingor pulsing form of active cell deformation called euglenidmotion or metaboly, which is effected by sliding of adjacentstrips.

Nutritional diversityEuglenids are notable for their diverse modes of nutrition,including:

• Phagotrophy (consumption of particles, especially othercells).

• Osmotrophy (absorbtion of organic molecules).• Photoautotrophy (photosynthesis).

Among the phagotrophs, there is a distinction drawn be-tween predominantly bacterivorous taxa, which have rigidpellicles with 12 or fewer strips and tend to be smaller in size,and predominantly eukaryovorous taxa that have pellicleswith many strips, are usually flexible, and tend to be larger.

Figure 2. Petalomonas— a bacterivorous benthic euglenid

The latter typically consume microbial eukaryotes, includ-ing unicellular algae.The bacterivores include the petalomonads (Petalomonadida),

which glidewith a forward-directed flagellum (e.g.,Petalomonas,Notosolenus) (Figs. 2, 3, 4), and ploeotiids, which glide onthe posterior/ventral flagellum (e.g., Ploeotia, Entosiphon)(Fig. 5).The eukaryovores include some taxa that glide primarily

on a forward-directed anterior flagellum An example is thewell-known genera Peranema (Fig. 6) and Anisonema (Fig.7).Photoautotrophic euglenids are phylogenetically less di-

verse than phagotrophs, although more species have beendescribed. Most are elongate, flexible cells that swim usingone or (more rarely) two emergent flagella (e.g., Eutrep-tia, Euglena, Eutreptiella). Other commonly encounteredspecies are rigid cells with various cell shapes (e.g., Phacus)and cells that are enclosed in an extracellular lorica but arenonetheless capable of swimming (Trachelomonas).Among the osmotrophs, there are primary osmotrophs (e.g.

2INTRODUCTION

Figure 3. Petalomonas— feasting on bacteria

Figure 4. Notosolenus

Figure 5. Ploeotia— a bacterivorous benthic euglenid

Figure 6. Peranema— a eukaryovores benthic euglenid

Figure 7. Anisonema— a eukaryovores benthic euglenid. Theone on the left has recently engulfed a diatom :(

3INTRODUCTION

Figure 8. Astasia— osmotrophic heterotrophic euglenid.

Astasia), which descended from within eukaryovorous lin-eages, and secondary osmotrophs, which are a collection ofspecies that descended from various photoautotrophs.

Euglenids are ambiregnalThe co-existence of phagotrophic and photoautotrophic speciesled to euglenids being examined both as plant-like and animal-like life-forms. This resulted in competing classificationschemes under the International Code of Botanical Nomen-clature and the International Code of Zoological Nomencla-ture— i.e., they are ambiregnal taxa.Of course euglenids are neither plant nor animal, so the

group does not fall neatly within the archaic plant-animal di-chotomy. Photoautotrophic euglenids in fact acquired pho-tosynthesis via a secondary endosymbiosis involving a chloro-plastidan green alga.

Practical importanceEuglenids are not known to cause disease in humans or live-stock.Several photoautotrophic and osmotrophic species are bloom-

formers in nutrient-rich conditions and are useful indicatorsof environmental pollution.Euglena sanguinea is a red coloured species is due to the

presence of astaxanthin and can be abundant enough tocolour water red.The pigment is used to protect the chloro-plasts from light that is too intense, but as the light levelschange the cells can take on a green colour as the red pig-ment is moved to the centre of the cells. Euglena sanguineais known to make the potent icthyotoxin euglenophycin.Phagotrophic species are ubiquitous primary consumers

and are likely to be important components of microbial foodwebs, especially in sediments.A few euglenids have been used as model systems for

addressing a wide variety of questions in basic cell biologyand physiology and as teaching aids. Euglena gracilis, for

Figure 9. Euglena sanguinea. Source.

Figure 10. Euglena sanguinea bloom. Source.

instance, is familiar to nearly every student who has takena general biology course. Euglena gracilis can be grown ina wide range of conditions: autotrophically or heterotroph-ically on various carbon sources (or both), under a broadrange of pH values.

Characteristic features in a nutshell• A characteristic cell wall, termed pellicle, consistingof proteinaceous strips beneath the plasma membrane, as-sociated with microtubules. The pellicle strips are ori-ented longitudinally in bacterivorous euglenids and usu-ally helically in eukaryovorous, photoautotrophic, and os-motrophic euglenids. Pellicle is a most clear morpholog-ical synapomorph defining euglendids.

• Cells usually have two heterodynamic flagella that orig-inate within an anteriorly directed flagellar pocket. Oneflagellum extends anteriorly, called the dorsal flagellum;the other, the ventral flagelum, bends to run posteriorly.Inmost photoautotrophs, most osmotrophs, and a few phagotrophs,only the dorsal flagellum is emergent, while the ventralflagellum is reduced in length and confined to the flagellarpocket (or is absent altogether) (Fig. 11).

• The flagellar pocket in photoautotrophic species is mod-ified into a reservoir (equivalent to the flagellar pocketsensu stricto) (Fig. 11) and a narrower cylindrical-shaped

4CHARACTERISTIC FEATURES IN A NUTSHELL

Figure 11. Characteristic traits in euglenids. (a) Petalomonad (phagotroph), (b) ploeotiid (phagotroph; note thickness of theventral/posterior flagellum), (c, d) anisonemids (phagotrophs), (e) Euglena (phototroph). All cells between 20 and 50 μm. Source:[Leander et al.(2017)Leander, Lax, Karnkowska, and Simpson].

canal leading to the exterior of the cell. Freshwater lin-eages have contractile vacuoles associated with the reser-voir.

• The flagella are thickened, sometimes extremely so, dueto the presence of paraxonemal (paraxial) rods.

• Photoautotrophic species have green plastids (chloroplasts)containing chlorophylls a and b. The plastids are sur-rounded by threemembranes and have thylakoids in stacksof three.

• Photoautotrophic species respond to the direction and in-tensity of light using a shading stigma (eyespot) and a pho-tosensory swelling at the base of the emergent flagellum.

• Cells have a feeding apparatus consisting of a tube orpocket reinforced longitudinally by microtubules. Thefeeding apparatus in many phagotrophs is further elabo-rated by four or five electrondense vanes and reinforcedby two robust rods partly composed of microtubules. Thefeeding apparatus in photoautotrophic and osmotrophicspecies is highly reduced.

• Threemodes ofmotility are seen, includingmetaboly, sub-strate mediated gliding, and swimming.

• Mitochondria have discoidal (paddle-shaped) cristae (asin other euglenozoans).

• The nucleus has permanently condensed chromosomesand a conspicuous nucleolus.

• The main storage polymer of most euglenids (perhaps all)is paramylon, a distinctive β-1,3-glucan. Cytoplasmicparamylon granulesmay be small or very large, especiallyin some photoautotrophic species. (Fig. 11)

Pellicle and metabolyThe cell wall of of euglenids, called pellicle is quite aunique invention. Commonly as strong cell wall is useful toprotect the cell. However, a strong armour makes the cellrigid. Euglenids have solved this dilemma with the pellicle—a strong cell wall, which nevertheless can retain flexibility

Figure 12. Euglenid pellicle and the associated stripes underSEM (left) and TEM (right).

to that the cells can move almost like amoeba. The pellicleof some euglenids has secondarily become rigid.The pellicle is comprised of parallel proteinaceous strips

(Figs. 12, 15), underlain by microtubules, that run along thelength of the cell. The number of individual strips variesfrom 4 or 5 in some petalomonads to 120 in some very largeeuglenophytes. When stripes are few, they tend to be thickerand are readily visible in light microscope. To see the moredelicate stripes, we need something else, like the electronmicroscope.The strips are composed mostly of a family of proteins

called articulins. The main frame of each pellicle strip is“S-shaped” in cross section and consists of an arch regionand a heel region that defines a groove (Fig. 14). Adjacentstrips articulate along their lateral margins. The strip archoverlaps with the heel of a neighbouring strip, giving thesurface of euglenid cells a striated appearance.The articulation zones between adjacent strips allow the

dynamic changes in cell shape called metaboly, euglenoidmotion, or euglenoid movement (Fig. 16). Euglenidswith more delicate strips tend to demonstrate more dramaticdegrees of metaboly, those with robust strips tend to be rigid,or nearly so.What is the point, meaning or ecological benefit ofmetaboly

remains a mystery. It is thought to facilitate the ingestion

5PELLICLE AND METABOLY

Figure 13. Large close up of an Euglena cell under lightmicroscope. Note the clearly visible pellicle stripes. Thecolourless central area is where the nucleus is. Also the whiteparamylon granules are nicely visible.

of large food particles, such as other eukaryotic cells, ineukaryovorous phagotrophs.Prior to cell division, the number of pellicle strips around

the cell periphery doubles. Each daughter cell (usually) in-herits the same number of pellicle strips as the parent cell ina semiconservative manner.

Cell structures

Flagella and locomotionMost euglenids possess two heterodynamic flagellathat emerge from the flagellar pocket. Some have highlyreduced flagella, giving the appearance of one or no flagellawhen viewed with the light microscope.

Paraxonemal rods

Euglenids possess paraxonemal rods or paraxial rodswithin the flagella that run alongside the 9 + 2 microtubularaxoneme (Fig. 18). The paraxonemal rods make euglenidflagella conspicuously thick when viewed under the lightmicroscope. The thickest flagellum can approach or exceed1 μm width in many larger cells.The paraxonemal rod in each flagellum has a different

structure: the rod in the ventral flagellum has a lattice likestructure, and the rod in the dorsal flagellum has, at core, awhorled structure that appears tubular in transverse sections.What is the role of the paraxonemal rods — I have no

idea.

Flagella hair

Euglenid flagella characteristically have fine hairs, whichgenerally emerge in horizontal (or shallowly helical) rows oftufts associated with the flagellar axoneme and/or paraxone-

mal rod (Fig. 18). The hair typically lie oriented with theirdistal ends pointing toward the distal end of the flagellum(Fig. 19).

Gliding

Gliding on a substrate is a specific way of locomotion in avariety of heterotrophic euglenids that live in the benthos.One flagellum (i.e., the dorsal/anterior flagellum) is held

ahead of the cell, while the other flagellum (i.e., the ventral,recurrent, or posterior flagellum) bends backward and ex-tends posteriorly from the cell, often within a ventral grooveor sulcus.. The hairs and paraxonemal rods of these flagellafacilitate gliding motility across substrates.In petalomonads and peranemids, the dorsal/anterior flag-

ellum is involved in gliding. During this gliding most ofthe anterior flagellum is held stiffly against the substrate,but the tip is in constant motion and functions as a sensoryapparatus. In these cells the posterior/ventral flagellum isshorter and thinner than the anterior flagellum. In somecases it lacks a paraxonemal rod, does not emerge from thereservoir, or is completely absent.In ploeotiids and anisonemids, only the posterior flagel-

lum is involved in gliding, and the whole anterior flagellumsweeps from side to side, In these cells the anterior flagel-lum is almost always thinner and usually shorter than theposterior flagellum.Some phagotrophic euglenids also use the anterior flagel-

lum like a hook to shovel prey cells into the feeding appara-tus.

Swimming

Most osmotrophic and photoautotrophic euglenids primarilymove using swimming motility. They usually possess anemergent dorsal flagellum that extends from the canal andis highly dynamic, while the reduced ventral flagellum doesnot emerge from the canal and is inactive.The emergent flagellum beats in an organised and con-

sistent pattern that takes the form of a “figure-eight” or alasso. This beat pattern pulls the euglenid cell through thewater column. By contrast, eutreptialean photoautotrophspossess two emergent flagella that both beat during swim-ming (some primary osmotrophs also have two emergentflagella).

Feeding apparatusPhagotrophic euglenids have feeding apparatuses that rangefrom relatively simplemicrotubule-reinforced pockets or tubesto highly complex systems of rods and vanes.Ploeotiids (e.g., Ploeotia andEntosiphon) and eukaryovorus

euglenids possess feeding apparatuses that are much morecomplex (Fig. 21). These include robust rods composed of

6CELL STRUCTURES

Figure 14. A general organization of pellicle ultrastructure in flexible photoautotrophic euglenids. Left: The configuration of three stripsand associated microtubules positioned beneath the plasma membrane and subtended by tubular cisternae of endoplasmic reticulum. Right:A pellicle strip with robust toothlike prearticular projections and robust postarticular projections (e.g., some Lepocinclis). Source:[Leander et al.(2017)Leander, Lax, Karnkowska, and Simpson]

Figure 15. SEM micrographs showing the diversity of pellicle structure in rigid photosynthetic euglenids (a-e) and primary osmotrophs(f). (a) Monomorphina. (b) Phacus. (c) Phacus. (d) Lepocinclis. (e) Phacus. (f) Rhabdomonas. All cells between 20 and 60 μm. Source:[Leander et al.(2017)Leander, Lax, Karnkowska, and Simpson]

Figure 16. A cartoon showing the euglenoid movement

ordered arrays of microtubules embedded within an amor-phous matrix (Fig. 20).Although most phagotrophic euglenids ingest their prey

whole, some euglenids (e.g., Peranema) can also feed bymyzocytosis. This mode of feeding is vampire-like, inthat the feeding rods pierce the prey cell, allowing the cellcontents to be sucked into a phagosomal vacuole within theeuglenid.The feeding apparatuses present in photoautotrophic and

osmotrophic euglenids are highly reduced, correspondingto the switch from predominantly phagotrophic modes ofnutrition to photoautotrophy and surface absorption, respec-

Figure 17. Left: three light micrographs of a cell of Astasia sp.,illustrating the process of metaboly (euglenoid movement) in thisparticularly flexible euglenid. Right: scanning electronmicrograph of Distigma sp., showing metaboly, and multipledistortions of the helical organisation of the pellicle due to slidingof adjacent strips. Source:[Leander et al.(2017)Leander, Lax, Karnkowska, and Simpson]

7CELL STRUCTURES

Figure 18. Euglenid paraxonemal rods in EM (left), andschematically (right).

Figure 19. Euglenid flagellar hair, pointing towards the tip ofthe flagellum.

Figure 20. The feeding apparatus of Entosiphon sulcatum inTEM. Not the three microtubular rods.

Figure 21. Entosiphon sulcatum. The feeding apparatus is seenas a funnel like rods in the cell anterior.

Figure 22. Phacus— a planktonic photosynthetic euglenid. Ahuge brigt pyrenoid is nicely visible in the middle.

tively.

PlastidsPhotoautotrophic euglenids or Euglenophyceae, are a mono-phyletic group, evolved once from eukaryovorous euglenidancestors that established a secondary endosymbiosis withgreen algal prey cells — probably a prasinophyte like Pyra-mimonas. This is reflected in the pigment composition ofeuglenids — they are green (chlorophylls a and b), as aregreen algae.Plastids are surrounded by three membranes, and possess

thylakoids in stacks of three). Most euglenid plastids con-tain a conspicuous pyrenoid (a region containingRuBisCOprotein) (Fig. 22), although the small disc-shaped plastidsof other species lack pyrenoids.Carbohydrate storage in the form of paramylon granules

is also often associated with the pyrenoids, but is also dis-tributed throughout the cytoplasm (Fig. 23).Some photosynthetic euglenids switch nutritional modes

and survive in the dark, whereby the plastids become bleachedover time. Several different groups of photosynthetic eu-glenids include species that have independently lost photo-synthesis (e.g., Euglena quartana, Euglena longa, Lepocin-

8CELL STRUCTURES

Figure 23. Euglena. Plastids are numerous and elliptical, puregreen in colour like in green algae. Close to the flagella pocket isa huge orange eyespot. The nucleus is central and large (lightarea in the middle). Large elliptical O-ring shaped paramylongranules are within the cytoplasm .

Figure 24. Phototaxis in Euglena. In the darkness theswimming pattern is random. Low light stimulates swimmingtowards the light (positive phototaxis), strong light away fromlight (negative phototasis).

clis cyclidiopsis).

PhotoreceptionEuglenophytes can respond to the intensity and direction oflight and orient themselves in the water column accordingly— i.e. they are phototactic (Figs. 24, 25).

Photoreception is accomplished by an apparatus consist-ing of a photo-sensory swelling at the base of the emergentdorsal flagellum and a closely associated shading structurecomposed of orange or red carotenoids, called the stigmaor eyespot (Fig. 23, 37).The stigma of euglenids is positioned near the base of the

Figure 25. Photoreceptor apparatus in Euglena, consisting of anexpanded reservoir, a canal, a paraflagellar swelling near the baseof the emergent flagellum, and a shading eyespot. Source:[Leander et al.(2017)Leander, Lax, Karnkowska, and Simpson].

Figure 26. Euglenid mitochondrion. Note the discoidalpaddle-shaped crista.

flagellar pocket/reservoir. In euglenids the stigma lies in thecytoplasm, not embedded within the plastid as in many otherphotosensory algae (e.g., within the green algae, dinoflagel-lates, and chrysophyceans).The stigma shades one side of the flagellar swelling. As

the cell rotates through the water, the swelling can detect thedirection of the most intense light source. The behaviourof the swimming flagellum will then respond in a way thatallows the cell to maintain a position in the water columnthat is best for photosynthesis.

MitochondrionThe mitochondria are distinctive in having stalked, paddle-shaped cristae, usually referred to as discoidal cristae(Fig. 26). This feature is shared byKinetoplastea, the sister-group of euglenids, and probably alsoHeterolobosea, a sister-group of Euglonozoa.Sometimes the taxa having distinctive discoidmitochondi-

ral cristae are referred as a formal taxon (kingdom) — Dis-cicristatae, within the eucaryotic super-group Excavata.The mitochondrion of Euglena gracilis forms a large retic-

ulated network. This conformationmay bewidespread amongeuglenids, although numerous separate elongated mitochon-dria are reported in some taxa.

HabitatsPhototrophic euglenids. mainly inhabit the water columnof freshwater environments. Very large and vermiform specieshave reduced flagella and often inhabit the interface betweenthe sediment and water column. Common species in fresh-water lakes and ponds are Trachelomonas, Phacus, Euglena.Only a few phototrophs inhabit the marine plankton, e.g.,

theEutreptiales. Several species are found in brackishwaterand estuaries (e.g. Eutreptiella), either in sediments or in thewater column.

9HABITATS

Phagotrophic euglenids. are widespread in marine, brack-ish, and freshwater sediments. The cells glide within thespaces between sand grains and within the narrow interfacebetween mud and the water column. They can compose upto 85% of the biomass of bacterivorous flagellates in certainaerobic freshwater, marine, and brackish sediments and arepresumably important predators in these ecosystems.Phagotrophic euglenids are mostly raptorial feeders (i.e.,

consume cytoplasm and organelles from large ruptured cells)on othermicrobial cells, although it is documented that someact as detritivores.Phagotrophic euglenids can be divided into bacterivores

and eukaryovores, based on morphological correlates offood preference. The bacterivores (petalomonads and ploeoti-ids) are rigid cells with few pellicular strips and tend to berelatively small (most are <25 μm long). The rigidity of thepellicle constrains them by gape limitation, thus they feedon small prey, primarily prokaryotes.The eukaryvores (e.g., “peranemids” and “anisonemids”)

are mostly slightly-to-highly flexible cells with unfused andmore numerous pellicular strips, and they also tend to belarger (most are >20 μm long). As a consequence, they aretypically capable of consuming larger prey items in bothabsolute and relative terms, such as large eukaryotic cells.E.g. Peranema trichophorum can engulf whole Euglenagracilis cell, which are almost as large as themselves. Sev-eral eukaryovorous euglenids specialise in consuming ben-thic microalgae, especially pennate diatoms (e.g. Fig. 7).

Euglenophyte examplesFigs of heterotrophic egulenids were shown above; here I in-troduce some of themore common photosynthetic euglenids,termed euglenophytes (note the –phytes suffix, which refersto plant-like metabolism).

TrachelomonasTrachelomonas produce a globular organic lorica that maybe smooth or decorated with spines. The lorica has a singleopening for the flagellum, and the cells locomote by swim-ming (Fig. 27). The primary component of the lorica is mu-cus, and during its development, the lorica slowly becomesthicker and ornamented. Iron and manganese are the mainnutrients necessary for the lorica formation, and thereforethe cell appears dark brown under light microscope (Fig.28).As the lorica is strongly mineralised, it becomes quite

fragile and can brake under mechanical pressure (Fig. 29)The sister group to the loricates is Colacium, which also

has the ability to produce copious amounts of mucus.

Figure 27. Trachelomonas showing the brownish color of thelorica. On the right, the optical focus is to the middle of the cell,showing the green colour of plastids and the red eyespot.

Figure 28. Trachelomonas, a schematic drawing and a SEMimage, nicely showing the opening in the lorica where theflagellum comes out.

Figure 29. The lorica of Trachelomonas is mineralised, andtherefore fragile, and can brake under mechanical pressure.

10EUGLENOPHYTE EXAMPLES

Figure 30. A scheme of Colacium, showing the overall structureof the colony, and a close-up of a terminal branc.

Figure 31. Colacioum colonies under phase contrast lightmicroscope. In phase contrast, the stalks are nicely visible.

ColaciumColacium is one of the few colonial examples of euglenidsand is widespread in aquatic substrates. It forms mucilagi-nous stalks and dendroid colonies, where the cells occur atthe ends of branched (Fig. 30, 31, 32).The cells attach by the anterior end, and secrete a stalk

composed of carbohydrate. Subsequent cell division yieldsnew branched colonies. The characteristic stalk is formed ofcarbohydrate extruded from the cell anterior in the form ofGolgi-generated mucocysts. More than one hundred muco-cysts may accumulate within the anterior of each cell priorto their excretion.Such colonies are functionally sessile, attached to a sub-

strate and the cells are not motile. In the sessile stage, flag-ella are non-emergent, but individual cells may produce anemergent flagellum and swim away to start a new colonyelsewhere.

Figure 32. A close-up of parts of Colacioum colonies

Figure 33. A planktonic rotifer, Keratella cochlearis, is badlycovered with Colacium. Hard to imagine that the zooplanktonwould benefit anything from such behaviour.

Figure 34. Left: Phacus triqueter. The cross section illustratesthe strongly flattened cell. Right: Phacus pleuronectes, smallelliptical chloroplasts and red eyespot are nicely visible.

Ironically, there seems to be a tendency for the colonies toattach to bodies of planktonic mesozooplankton (Fig. 33).

PhacusPhacus is a common freshwater planktonic euglenid. Cellsare oval to nearly circular and are highly flattened (Fig. 34).Phacus has a rigid pellicle and metaboly is never observed.Plastids are small, elliptical and numerous.Common Phacus tortus is distinctive with its twisted cell

(Fig. 35).Some Phacus species have a fairly rough cell surface cov-

ering (Fig. 36).

EuglenaEuglena is the best-known euglenoid genus, with >150 de-scribed species. Euglena is characterized by the presence ofa single emergent flagellum. Plastid shape is variable butoften discoidal, and cells are cylindrical (not flattened) incross section. Most Euglena species are elongated, with arounded anterior and the posterior tapered to a point (Fig.23, 37).A dozen or so species produce red granules in numbers

sufficient to give cells a bright or brick-red appearance (Fig.9), resulting from large amounts of the carotenoid astaxanthin.

11EUGLENOPHYTE EXAMPLES

Figure 35. Left: Phacus tortus. The cell is distinctively twisted.

Figure 36. Phacus monilatus with a highly structured cell wall.

Figure 37. Euglena— perhaos the most known photosyntheticeuglenid.

Figure 38. Eutreptiella

When large populations of cells are present, they may formdramatic, blood-red surface scums on ponds or other waterbodies (Fig. 10). The formation of such scums is favored bythe presence of high levels of dissolved organic compoundsand high temperatures.Cells of some species appear red most of the time, but

those of several species can change from green to red within5–l0 minutes in response to increased light intensity such asat sunrise, then return to green coloration at the appearanceof a cloud or at sunset.This color change involves differential positioning of the

red globules and green plastids at the centre and periphery ofcells. When the red globules are at the cell periphery, cellsappear red; when the red globules occupy a central position,surrounded by green plastids, cells appear green. Euglenasanguinea is the commonest of the red species (Fig. 10).

EutreptiellaEutreptia and Eutreptiella are found in fresh, brackish, andmarine waters, where they sometimes forms blooms. Eu-treptia has two equal flagella, while Eutreptiella has towunequal flagella (Fig. 38). Eutreptiella is also common andforms occasional blooms in the Baltic Sea.Eutreptiella has a very flexible cell wall and can change

shape from spherical to long elongate (Figs. 38, 39). One ofthe species, Eutreptiella gymnasica, common in the BalticSea, has even a name referring to metaboly.

Acknowledgments

References[Leander et al.(2017)Leander, Lax, Karnkowska, and Simpson] Brian S.

Leander, Gordon Lax, Anna Karnkowska, and AlastairG. B. Simpson. Euglenida. In John M. Archibald,

12REFERENCES

Figure 39. Through metaboly, Eutreptiella cells can change theshape from spherical to highly elongate and everything inbetween

Alastair G.B. Simpson, and Claudio H. Slamovits,editors, Handbook of the Protists, pages 1047–1088.Springer International Publishing, Cham, 2017.ISBN 978-3-319-28147-6 978-3-319-28149-0. doi:10.1007/978-3-319-28149-0_13. URL http://link.springer.com/10.1007/978-3-319-28149-0_13.

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