Pluripotency and the origin of animal multicellularity

“Evolution of life on Earth” has been among the various topics discussed in these GEITP pages, because gene-environment interactions play a major role in how organisms (all living things) continue to evolve — i.e. in response to advantageous, or adverse, environmental signals. The title of this email maybe needs explanation? ☹ “Pluripotency” as it is related to animal multicellularity (having numerous cells, and different cell-types) is defined as “capacity to develop into any type of cell or tissue — except those that form placenta or embryo.” The last common ancestor (LCA) of all living animals appears to have had (at the minimum) epithelial (outer surface) and mesenchymal (capacity to develop into tissues of lymphatic and circulatory systems — as well as bone, muscle and cartilage, but here it simply means ‘non-epithelial) cell-types that could trans-differentiate within an ontogenetic (origination and development of an organism, from time of fertilization of egg to organism’s mature form) life cycle. This life cycle would require the ability to regulate spatial and temporal gene expression, and would include a diversified set of signaling pathways, transcription factors, enhancers, promoters and non-coding RNAs [see attached article, Fig. 1].

Recent analyses reveal that — even unicellular holozoans (organisms that include animals and their closest single-celled relatives, but exclude fungi) — use similar gene regulatory mechanisms to transit through the different cell states that comprise their life cycles, suggesting that early metazoans (all animals having a body composed of cells differentiated into tissues/organs, and usually a digestive cavity lined with specialized cells) were more complex than has generally been thought. To test whether choanocytes [cells having flagella (slender thread-like structures that enable many protozoa, bacteria, spermatozoa, etc.) to swim, even sponges are in this category] and choanoflagellates (group of free-living unicellular and colonial flagellates, considered to be closest living relatives of animals) — accurately reflect the ancestral animal cell-type, authors [see attached article] first compared cell-type-specific transcriptomes (all mRNA transcribed from ‘active’ genes) from a sponge, with transcriptomes expressed during the life cycles of a choanoflagellate, and two other sponges [see Fig. 1 of attached].

These three sponge somatic cell-types were chosen because they are hypothesized to be homologous to cells present in the LCA of contemporary metazoans, choanozoans or holozoans: (i) choanocytes (having internal feeding cells that capture food by pumping water through the sponge); (ii) pinacocytes (having cells that line internal canals and the outside of sponge); and (iii) archeocytes (mesenchymal pluripotent stem cells that inhabit the middle collagenous layer and have a range of other functions).

Authors thus compared the transcriptomes, fates, and behaviors of these three primary sponge cell-types (choanocytes, pluripotent mesenchymal archaeocytes, and epithelial pinacocytes) — with choanoflagellates and the other unicellular holozoans [see Figures 2,3,4 of attached]. Unexpectedly, they discovered that the transcriptome of sponge choanocytes is the least similar to the transcriptomes of choanoflagellates; the transcriptome of sponge choanocytes is significantly enriched in genes unique to either animals or sponges alone. In contrast, pluripotent archaeocytes up-regulate genes that control cell proliferation and gene expression, similar to functions of other metazoan stem cells and in the proliferating stages of two unicellular holozoans — including a colonial choanoflagellate. Choanocytes in the sponge exist in a transient metastable state and readily trans-differentiate into archaeocytes, which can then differentiate into a range of other cell-types. These sponge cell-type conversions are similar to the temporal cell-state changes that occur in unicellular holozoans.

Together, these analyses argue against homology of sponge choanocytes and choanoflagellates, and the view that the first multicellular animals were “simple balls of cells with limited capacity to differentiate.” Instead, these data are consistent with the first animal cell being able to transition between multiple states — in a manner similar to modern trans-differentiating and stem cells in higher animals. 😊


Nature 27 June 2o19; 570: 519-522

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