Origins of Eukaryotic Multicellularity
Above the evolutionary time, cells of multicellular organisms evolved a series of states (cell types). The mechanisms that lead to the formation of such states are unknown. Biology includes several competing hypotheses on the origin of eukaryotic multicellularity; all of them based on observations made on the behavior of current species. These hypotheses suggest multiple pathways that can lead to multicellular organisms; some pathways more successful than others. Moreover, these competing hypotheses may all be valid. Note that only a few general notions are mentioned here.
1.13.1 Colonies Inside an Early Unicellular Common Ancestor
One of the hypotheses for multicellularity suggests a repeated division of the nucleus within the same unicellular organism and a subsequent formation of membranes in between the nuclei. A reminiscent coenocytic behavior can be seen in multicellular eukaryotic organisms, for instance, in the eggs (0.51 ± 0.003 mm) laid by the well-known Drosophila melanogaster (vinegar fly). The initial stages of the vinegar fly eggs contain multiple nuclei in a common cytoplasmic space (the entire volume of the egg) [143]. Only a few stages of development later, the cell membranes around the floating nuclei start to appear almost simultaneously to constitute the initial cells of the larva [143].
1.13.2 Colonies of Early Unicellular Common Ancestors
A second hypothesis for the origin of multicellularity proposes that unicellular organisms may aggregate to form unitary colonies that can achieve multicellularity and cell specialization over time. According to this theory, multicellularity emerged from cooperation between unicellular organisms. Examples of cooperation among organisms have been observed in nature at different scales and in various forms. One of the simplest integrated multicellular organisms is Tetrabaena socialis in which four identical cells constitute the individual [144]. The nuclear genome of T. socialis dictates the number of cells in the colony [145]. Another example is the choanoflagellate (Greek and Latin – khoánē, “funnel”; flagellate, “flagellum”) Salpingoeca rosetta, which can exist as a unicellular organism or it can switch to form multicellular spherical colonies called rosettes (form bridges between cells by incomplete cytokinesis), showing a primitive level of cell differentiation and specialization. Formation of multicellular colonies is induced by different signal molecules. The source of such signal molecules can originate from individuals of the same species (i.e. slime molds) or from individuals of different species (i.e. bacterium species) [146]. In the case of S. rosetta, the signal molecules for colony formation originates from the food source, namely the Algoriphagus machipongonensis bacterium (phylum Bacteroidetes) [147, 148]. Choanoflagellates, sponges and algae of the genus Volvox are more complex examples of first evolutionary stages that indicate the border between colonial organisms and multicellular organisms. Choanoflagellates are the closest relative of metazoans (all animals composed of cells differentiated into tissues and organs) [149, 150]. Some genes required for multicellularity in animals, such as genes for adhesion, genes for signaling, and genes for extracellular matrix formation, are also found in choanoflagellates [151]. This suggests that these genes may have evolved in a common ancestor before the transition to multicellularity in animals [152]. Sponges are one of the oldest primitive multicellular organisms in the fossil record. Choanoflagellates are small single-celled protists, partially similar in shape and function with some of the sponges cells (choanocytes) [153]. Many associations have been made in the past between choanocytes and choanoflagellates. However, the transcriptome of sponge choanocytes is the least similar to the transcriptomes of choanoflagellates and is significantly enriched in genes unique to either animals or sponges alone [154]. Slime molds are also interesting examples, which can indicate how some multicellular organisms formed. Slime molds are unrelated eukaryotic organisms that can live as single cells. In certain conditions (i.e. starvation), single cells of the same species can aggregate to form multicellular reproductive structures [155]. For instance, the multicellular aggregate (a slug-like mass of a few thousand cells called a grex) of amoebae Dictyostelium discoideum can show cellular adhesion, cellular specialization, tissue organization, and coordination that allows for mechanical movement [156, 157]. Although the behavior of D. discoideum is not necessarily a close example of the process that led to multicellular organisms, it can certainly serve as a clue for detailed research on the emergence of multicellularity.
1.13.3 Colonies of Inseparable Early Unicellular Common Ancestors
A third hypothesis for the origin of multicellularity suggests an early unicellular organism that underwent repeated divisions with incomplete separations between generations, which further led to a forced cooperation and specialization for a primitive tissue formation. Plant embryos and animal embryos adhere to this behavior. More to the point, the eukaryotic microorganism Saccharomyces cerevisiae (the budding yeast) is an ideal example for this hypothesis [158]. Yeast colonies growing on solid media show specific structural patterns in their three-dimensional multicellular organization. These structural patterns are specific to each yeast strain [159]. Moreover, variations in the multicellular organization appear to be dependent on the environmental parameters, such as the position of surrounding cells, nutrient gradients, temperature, and so on [160].
1.13.4 Chimerism and Mosaicism
The cooperation of eukaryotic cells is best observed in the case of two phenomena, namely chimerism and mosaicism. Mosaicism is represented by two or more cell populations in different tissues originating from one fertilized egg. Namely, one cell population with the original genotype (usually representing the majority) and other cell populations with slight variations of the original genotype. One of the mechanisms that lead to mosaicism is represented by transposomes [161]. With embryonic development, the genotype of an organism can undergo various types of mutations, including transposome-induced mutations above different cell lines. These mutations can occur late in embriogenesis, leading to marginal effects at the organism level, or they can occur early in the embryonic development of an organism with more pronounced/noticeable effects [162]. Transposome-induced mutations represent a normal and nonrandom variability in multicellular organisms, leading to different phenotypic characteristics [161]. The classic example, however, is represented by the experiment performed by Barbara McClintock on corn kernels, where the transposomes inactivate the gene for the pigment protein and the phenotype is easily recognizable (please see the “horizontal gene transfer” subchapter from above). Mosaicism can also be represented by other types of mutations. For example, in humans, Down syndrome is characterized by an additional copy of chromosome 21, which is frequently attached to chromosome 14 (Trisomy 21). The extra copy of chromosome 21 slightly changes the chromosomal territories in the cell nucleus and the way heterochromatin and euchromatin are distributed. This leads to unusual variations in the expression of certain genes, especially those present on the extra chromosome 21 and those present on the neighboring chromosomal territories. Trisomy 21 occurs at the beginning of embryogenesis. However, such a mutation may appear late in embryogenesis, which results in mosaic tissues, part with normal cells and part with cells with an extra copy of chromosome 21 [163, 164]. Such a mosaic can be clinically unnoticeable unless genetic analysis is made on different tissues of the organism. Moreover, it is believed that a combination of germinal and somatic Trisomy 21 mosaicism may be reasonably common in the general population [163]. In development, cells with different genotypes compete in the tissue population. Such a competition can lead to the possibility (especially for mosaicism that appeared late in embryogenesis) in which cells with the original genotype completely marginalize the function of mosaic genotypes or vice versa, depending on which is more fit for a specific function. On the other hand, chimerism is represented by fusion of more than one fertilized zygote, namely cells of different organisms that are orchestrated by common molecular signals to form a single body [165]. Chimerism can be observed in all multicellular species to a greater or lesser extent and may be accompanied by genetic mosaicism in any of the genotypes that form the composite organism.
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