Darwin’s Green Living Fossil: The Microalga Cyanophora paradoxa and Evolutionary Stasis

In 1723, Anthonie van Leeuwenhoek, the "master of fleas and father of microbiology", died at the age of 90 [...].

Here, we will focus on C. paradoxa, a new genus and new species.Figure 1A shows the original drawings from the article by Korschikov, 1924 [2].The author characterized his nova species (and new genus) in the following words (translated into English): A typical individual of C. paradoxa is 6 to 9 micro-meters long and is equipped with 2 flagella, one of which is much shorter than the other; the only contractile vacuole is in the rear part, and the nucleus is in the front region of the cell.In the center of the microbe, two large green bodies are visible, which contain a colorless, dense granum.Starch grains are detectable in the cytoplasm, often in the vicinity of the nucleus.The green bodies divide, reminiscent of microbes of the genus Chroococcus.
C. paradoxa reproduces via longitudinal cell division, usually when the aquatic organism swims around with the aid of its motile flagella.The green bodies are equally distributed among the dividing cells.Sometimes, encystation is observed: the protoplast becomes round, the nucleus moves to the center of the cell and the contractile vacuole disappears.Starch is stored in large granules; a thin wall surrounds the rest of the cell.A typical individual of C. paradoxa is 6 to 9 micro-meters long and is equipped with 2 flagella, one of which is much shorter than the other; the only contractile vacuole is in the rear part, and the nucleus is in the front region of the cell.In the center of the microbe, two large green bodies are visible, which contain a colorless, dense granum.Starch grains are detectable in the cytoplasm, often in the vicinity of the nucleus.The green bodies divide, reminiscent of microbes of the genus Chroococcus.
C. paradoxa reproduces via longitudinal cell division, usually when the aquatic organism swims around with the aid of its motile flagella.The green bodies are equally distributed among the dividing cells.Sometimes, encystation is observed: the protoplast becomes round, the nucleus moves to the center of the cell and the contractile vacuole disappears.Starch is stored in large granules; a thin wall surrounds the rest of the cell.
The colored bodies should not be interpreted as chromatophores (chloroplasts); rather, they represent independent organisms.One can squeeze them out of the host organism, and thereafter they remain, cultivated in aqueous solutions, intact over long time periods.Hence, the green bodies are independent organisms, which live in symbiosis with the colorless flagellate.The nature of these symbionts remains elusive.However, they are reminiscent to cyanophyceen (i.e., Cyanobacteria), but concerning their structure, they differ from typical blue-green algae.In summary, C. paradoxa must be viewed as an organism sui generis, i.e., a unique one of a kind, with no analogy to any other living being known so far.
Locus typicus: Region Charkow; occurs in small muddy waters, but never at high density.
Decades later, Steiner and Löffelhardt [5] and other biologists interpreted C. paradoxa (Figure 1A-C), the best-studied species within the glaucophyte algae (Glaucophyta, one The colored bodies should not be interpreted as chromatophores (chloroplasts); rather, they represent independent organisms.One can squeeze them out of the host organism, and thereafter they remain, cultivated in aqueous solutions, intact over long time periods.Hence, the green bodies are independent organisms, which live in symbiosis with the colorless flagellate.The nature of these symbionts remains elusive.However, they are reminiscent to cyanophyceen (i.e., Cyanobacteria), but concerning their structure, they differ from typical blue-green algae.In summary, C. paradoxa must be viewed as an organism sui generis, i.e., a unique one of a kind, with no analogy to any other living being known so far.
Locus typicus: Region Charkow; occurs in small muddy waters, but never at high density.
These authors argued that the two "green intracellular bodies" are the "plastids" of C. paradoxa, because "the transition from endosymbiont to organelle has certainly taken place", [5].In order to emphasize the plastid nature of the "cyanelle", alternative names have been coined, such as "cyanoplast" or "muroplast".The third term signifies that the "cyanelle" is surrounded by a prokaryote-like peptidoglycan wall.This "Living Fossil" may "mimic an early stage in organelle evolution" and, hence, is strong proof of the "en-dosymbiotic theory", describing and explaining the origin of plastids in green eukaryotes (algae, plants, i.e., the Viridiplantae; see [7,8]).
Ten years after Steiner and Löffelhardt's account, Price et al. [3] published the draft nuclear genome and part of the proteome of C. paradoxa (the sequence of the cyanelle genome, which is of similar size to that of typical chloroplasts, has been known since 1995).Based on these data, there is strong evidence for a single evolutionary origin of the primary plastids in the "Supergroup Plantae".In addition, the hypothesis emerged that the glaucophytes may not be a lineage which should be interpreted as "Living Fossils".The reasons for this surprising statement are as follows: In addition to the "primitive" peptidoglycan wall that surrounds the cyanelles, C. paradoxa has several derived traits, such as a modern pathway for starch biosynthesis and sophisticated plastid protein-import machinery.Nevertheless, the nuclear genome of C. paradoxa contains a signal of cyanobacterial ancestry.
Moreover, some key genes responsible for starch biosynthesis were found to be derived from prokaryotic "energy parasites", such as Chlamydiae.Price et al. [3] concluded that the C. paradoxa genome contains a unique combination of ancestral, novel, and borrowed (via horizontal gene-transfer-acquired) genes, like the genomes of members of the Kingdom Plantae.
In the most recent analysis of an improved C. paradoxa genome assembly, Price et al. [6] corroborate their earlier findings and conclude that this "paradox microorganism" is an important "model for understanding ancient events in algal evolution".Moreover, they speculate that "additional genomes of glaucophyte species (should be analyzed) to discover. ..ancient events driven by endosymbiosis in the ancestor of these taxa" [6].
In this context, studies on the cyanobacterium Anabaena sp. and C. paradoxa by Kato et al. [9,10], which analyzed the structure of photosystem I in these microorganisms, are of importance.
During oxygenic photosynthesis, solar energy is converted into chemical energy (stored, for instance, as starch grains).In addition, molecular oxygen (O 2 ) is generated via the light-mediated splitting of water (H 2 O).In all green oxygenic photosynthesizers, this light-driven energy conversion is carried out by two pigment-protein complexes (consisting of several subunits)-photosystem II (PS II, usually organized into a dimer) and PS I (diverse among photoautotrophic organisms) [11].
For instance, in the well-studied cyanobacterium Anabaena sp., the structure of the PSI tetramer, as well as the excitation energy transfer processes, upon photon absorbance, have been characterized in detail [9].In a subsequent study, Kato et al. [10] documented that the PSI tetramer isolated from the cyanelle of C. paradoxa displays a special monomer-monomer arrangement (and interaction) that differs considerably from that observed in the Anabaena tetramer [10].Moreover, the excitation energy transfer patterns in C. paradoxa PS I tetramers were found to be different from that in the cyanobacterium analyzed by the authors.
Based on these comparative studies (PS I in Anabaena sp. vs. C. paradoxa), Kato et al. [10] concluded that the "Cyanophora PS I represents an evolutionary turning-point between cyanobacteria and other photosynthetic eukaryotes" (such as algae and land plants).
In another section of their research paper, Kato et al. [10] argue that "Cyanophora is an intermediate between oxygenic photosynthetic prokaryotes and eukaryotes in the evolutionary processes of oxyphototrophs".More specifically, the authors drew the following far-reaching conclusion: "Cyanophora is evolved from cyanobacteria having PS I-trimers and tetramers, and subsequently serves as an ancestor for other eukaryotic algae where PS I becomes a monomer", and "Cyanophora PS I is in the middle of transition from cyanobacterial trimers and tetramers to eukaryotic monomers" [10].These statements raise the following question: How are "Living Fossils" defined?In his book On the Origin of Species, Darwin (1859) [12] wrote that "aberrant species", which "may fancifully be called 'living fossils',. . .will aid us in forming a picture of the ancient forms of life".As examples, Darwin [12] mentioned the "Ornithorhynchus"

Microorganisms 2024 , 5 Figure 1 .
Figure 1.Original drawings by A. Korschikov, 1924, depicting the aquatic microalga Cyanophora paradoxa (A).Adult individuals in the process of cell division (a-c) and a destroyed microorganism, showing two chromatophores (d).Fixed individual (e), start of encystment (f) and a fully developed cyst (g) (adapted from ref. [2]).Light micrograph of an adult, living, dividing individual of Cyanophora paradoxa (B) and a schematic drawing of this unicellular microalga (C).

Figure 1 .
Figure 1.Original drawings by A. Korschikov, 1924, depicting the aquatic microalga Cyanophora paradoxa (A).Adult individuals in the process of cell division (a-c) and a destroyed microorganism, showing two chromatophores (d).Fixed individual (e), start of encystment (f) and a fully developed cyst (g) (adapted from ref. [2]).Light micrograph of an adult, living, dividing individual of Cyanophora paradoxa (B) and a schematic drawing of this unicellular microalga (C).