Chapter 1 - The history of phycology and protistology: changing views on the origin and evolution of the Eukarya

becuase of their minute size, protists remained undiscovered until the development of the first microscopes. Howeever, while the fisrt primitive microscoped were built arount 1590 in the Netherlands, it was not until 1680 that the Dutch ….. described and drew the first protists, which he called…

Antoni Van Leeuwenhoek, Animalcula

in the1700s, protists did not feature in Linneaus Systema Naturae (1758). Only a single protist was listed, namely the colonial green alga…, which is vitible with the naked eye

Volvox (because of its motility, it was classified as an animal, not a plant)

the first systematic account of protist (then referred to as Infusoria) was by the Danish scientist

O.F. Muller (1786)

Protistological research took off in the 19th century, starting with the important systematic contributions of the Germans…

E. Haeckel and C.G. Ehrenberg

the first transmission electron microscope were developed in the… and became an important tool in protistological research (and cell biology in general), when techniques of specimen preparation improved.

early 1950s

the first scanning electron microscopes were developed in the … The use of electron microscopes signaled a significant breakthrough in protistological and phycological research. For the first time it was possible to study the ultrastructural detail of the cell features and organelles.

mid 1960s

In the 1960s protein sequences started to be used to infer phylogenetic relationships. It was soon clear however that no single protein sequence had the “search” to infer a universal tree of life. However, one particular type of RNA could do the job:

rRNA

rRNA molecules appeared to be excellent candidated for

reconstructing phylogenetic relationships between living organisms

By the late 1980s the rRNA of the small subunit (SSU) of the ribosome of representatives of all major groups of living organisms had been sequenced. Phylogenetic analysis of these sequences revealed a universal tree of life which led to a revolutionary revision of the evolution of life on earth. The most striking features of this SSU rDNA tree of life were:

1. there are 3 man domais: the Archaea, the Bacteria and the Eukarya

2. The eukaryal branch is characterized by long evolutionary distances, the presence of a nuber of early-branching lineages, and a crown group radiation

3. on the basis of ancient paralog proteins the root of the tree was placed in the bacterial branch, putting the Archaea and the Eukarya in a sister group relationship

SSU rDNA sequencing also proved beyond doubt that mitochondria and plastids were derived from bacteria and cyanobacteria respectively, as

mitochondrial and plastid SSU rDNA most closely matched the DNA of these prokaryotes.

the evolutionary model by the SSU rDNA tree has been seriously challenged during the last 15 yeara, mainly as a result of analyses of complete genomes in the wake of the next generation sequencing revolution. This has led to 2 important insights:

1. endosymbiotic events have played a pivotal role in the major evolutionary transitions in the eukaryotic tree of life, and probably also the actual origin of eukaryotes

2. lateral gene transfer (LGT) is most probably a far more important process than hitherto recognized, in prokaryotes but also in eukaryotes, and this process has not only driven important evolutionary transitions, but can also seriously disguise evolutionary relationships and thus complicate tneir reconstruction

Phylogenetic relationships have revealed that mitochondria arose from within the alfa-Proteobacteria (and probably share a common ancestor with the Rickettsiales). The Rickettsiaceae have obligate

intracellular life cycles. They also have the smallest genomes of all alpha-Proteobacteria, which is caused by reductive evolution, with a biased loss of genes.

off all eubacteria,… has the most mitochondrium-like genome

Rickettsia

In total, it is estimated that the alfa-Proteobacterial ancestor of the mitochondrion possessed one thousand or a few thousand genes. As in obligate intracellular organisms (such as parasited), a large number of these genes (1000-3000) have been lost from

the mitochondrial genome. Many genes however were transferred to and selectively maintained in the genome of the host. These nuclear genes are therefore alfa-Proteobacterial descendants. Their products are tergeted to the mitochondria, but most function in other subcellular compartments.

Not all eukaryotes possess a typical mitochondria. Some organisms possess

mitochondria which can produce ATP without using oxygen. Others have mitochondrion-like organelles whose exact relationship to mitochondria were not know until recently.

Yet other parasitic protists appear to have no mitochondria at all. The latter two groups were until recently commonly referred to as the Archezoa.

There are two classes of ideas on the origin of the eukaryotes:

• eukaryotic ancestor (which already possessed a nucleus and a cytoskeleton) took up a bacterial endiosymbiont which evolved into the mitochondrion

• the origin of the mitochondrion coincided with the origin of the eukaryotic cell

Plastids=

the light-harvesting organelles in photosynthetic protists, macroalgae and plants. They evolved from an intracellular cyanobacterium. They posses (just like mitochondria) their own circular genome, which encodes essential RNA’s and proteins. They also have their own ribosomes and divides by fission

Despite being complex structures, plastids have much in common, and it was therefore generally assumed that

all algae were closely related

The idea that the algae were necessarily related however was soon challenged. According to Mereschkowsky, plastids of differently pigmented groups of algae originated

independently from correspondingly pigmented bacteria. In addition, early ultrastructural investigations revealed that some groups of algae shared more (cytoplasmatic) features with non-photosynthetic organisms than with other algae. (this was most obvious in the euglenids whose platsids share a number of characteristic with green algae, while their flagellar apparatus was more akin to that found in parasitic and non-phyotosynthetic kinetoplastids)

the evolutionary complexity and plastid diversity is the result of various kinds of

endosymbioses: primary, secondary, teriary and maybe even quaternary ones.

• primary ES: involves the uptake of a cyanobacterium by a heterotrophic eukaryote

• Secondary and higher ES: involve the horizontal spread of plastids omong unrelated eukaryotic groups

Although photosynthetic organisms display a bewildering degree of genetic, biochemical and morphological diversity, all plastid-containing eukaryotes originally owe their photosynthetic appartus to

a single ancient endosymbiont between a (heterotrophic) eukaryote and a cyanobacterium, This ES gave rise to the so-called primary plastids (the exact nature of the cyanobacterial endosymbiont remains elusive because plastids show no obvious similarity or phylogenetic relationship to any one kind of cyanobacterium)

primary plastids are always locate in the cytosol and are bounded by

an envelope of two membranes which are homologous with the two membranes of the cyanobacterial envelope. (it is assumed that the phagosomal membrane around the plastid has been lost)

three types of algae have primary plastids:

• red algae (Rhodophyta)

• green algae (Chlorophyta)

• Glaucophyta

these plastids are sometimes referred to as rhodoplasts, chloroplasts, and cyanelles respectively.

because of their (plastid) difference in pigmentation and biochemical composition, it was not clear for a long time whether the primary ES even took place once or at several indepentent occasions. During the last years however, evidence has accumulated that the primary ES event took place

only one time, and the red, green and glaucophyte algae form a monophyletic group (this group is often referred to as the plants (Plantae), or more recently as the Archaeplastida)

The monophyly of the plastids is supported by several common features, such as:

• a similar gene content of plastid genomes

• presence of plastid-specific gene clusters

• orders that are distinct from those in the Cyanobacteria

• the conservation of the plastid-protein import machinery and protein-targeting signals

Like in mitochondria, the genome of the cyanobacterial symbiont has been strongly modified by the ES. Cyanobacteria encode thousands of genes, contemporary plastid genomes contain

between 50-200 protein-coding genes. Many genes have been lost, and most of the ones that had been retained have been transferred to the nucleus of the host, with the products of many of them being targeted to the plastids.

The plastid proteosome thus has about the same number of proteins (>1000) as a cyanobacterium.

Why is Paulinella chromatophora important in the evolution of plastids?

It represents a second, independent primary endosymbiosis, separate from the one that produced the primary plastids of plants and algae.

What kind of organism is P. chromatophora?

A testate amoeba belonging to the Cercozoa. “Testate” means it has a protective shell or covering.

How does P. ovalis differ from P. chromatophora?

P. ovalis lacks photosynthetic endosymbionts and eats cyanobacteria; P. chromatophora receives photosynthates from its chromatophores.

Photosynthesis is not the exclusive property of the green, red algae and the glaucophytes. Many other protist groups are photosynthetic. Yet none of these have acquired their plastids by

directly taking up a cyanobacterium. Instead, photosynthesis spread laterally across the eukaryotic tree by endosymbioses between two eukaryotes (heterotrophic host and an alga, not a cyanobacterium)

It is generally accepted that secondary ES happened at least three times and has involved both green and red algal endosymbionts. Secondary plastids are found in:

• The Chlorarachniophyta

• Euglenida

• must also have happend at least once with red algae, but whether the plastids observed in groups such as Stramenopiles, haptophytes, cryptophytes, Apicomplexa, dinoflagellates and some smaller are the direct result of a secondary endosymbioses or of a higher order ES is as yet uncertain

The plastids of the Stramenopiles, Haptophyta, Cryptophyceae, Apicomplexa and Chlorarachniophyta have 4 membranesm whereas those of the Euglenida and the dinoflagellates are bound by 3 membranes:

this is a natural consequence of eukaryotic phyagocytosis, and means that unlike primary plastids, secondary and higher order plastids reside in the lumen of the endomembrane system of the host, and not in its cytosol.

at the level of genes and proteins, the differences between the membranes of primary and secondary plastids have significant repercissions in gene transfer and protein trafficking. In algae with a primary plastid, most plastid proteins are encoded by .

the nucleus and are targeted to the plastids post-translationally using a specific transit peptide that is recognized by the plastid’s TOC/TIC import machinery.

In higher-order plastids, nuclear-encoded proteins targeted to the plastids must traverse one (or more) additional membranes. This involves additional complex pathways for protein trafficking, involving the endoplasmatic reticulum and specific signal peptides.

In a 4-membrane plastid, the space between the second and third membrane is called

the periplastid space, is derived from the cytosol of the (red or green) alga that has been taken up

een nucelomorf is het sterk verkleinde overblijfsel van de celkern van de opgenomen eukaryota alg bij secundaire ES, en dit is krachtig bewijs hier:

de opgenomen partner was een eukaryoot met een eigen celkern, en niet alleen een cyanobacterie.

In the two algael groups: cryptophytes and the chlorarachniophytes the nucleumoroh genome is very small, containing 487 and 284 protein-encoding genes respectively. Only a fraction of

these genes are targeted to the plastid (30-17 respectively). The remainder of the genes present in the nucleomorphs is for “housekeeping”. All the other plasti-targeted genes have been transferred to the nucleus of the host.