The most widely held, but rarely tested, hypothesis for the origin of animals is that they evolved from a unicellular ancestor with an apical cilium surrounded by a microvillar collar that structurally resembled modern sponge choanocytes and choanoflagellates 1-4. Here we test this traditional view of animal origins by comparing the transcriptomes, fates and behaviours of the three primary sponge cell types-choanocytes, pluripotent mesenchymal archeocytes and epithelial pinacocytes-with choanoflagellates and other unicellular holozoans. Unexpectedly, we find 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. In contrast, pluripotent archeocytes up-regulate genes controlling cell proliferation and gene expression, as in other metazoan stem cells and in the proliferating stages of two unicellular holozoans, including a colonial choanoflagellate. Choanocytes in the sponge Amphimedon queenslandica exist in a transient metastable state and readily transdifferentiate into archeocytes, which can 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 5. Together, these analyses offer no support for the homology of sponge choanocytes and choanoflagellates, nor for the view that the first multicellular animals were simple balls of cells with limited capacity to differentiate. Instead, our results are consistent with the first animal cell being able to transition between multiple states in a manner similar to modern transdifferentiating and stem cells. References 1 Cavalier-Smith, T. Origin of animal multicellularity: precursors, causes, consequences-the choanoflagellate/sponge transition, neurogenesis and the Cambrian explosion.
Main 46The last common ancestor of all living animals appears to have possessed epithelial and 47 mesenchymal cell types that could transdifferentiate over an ontogenetic life cycle 48 ( Fig.1a) 1,4 . This capacity to develop and differentiate required a regulatory capacity to 49 control spatial and temporal gene expression, and included a diversified set of signalling 50 pathways, transcription factors, enhancers, promoters and non-coding RNAs (Fig. 1a) [5][6][7][8][9] . 51Recent analyses of the genomes and life cycles of unicellular holozoan relatives of 52 animals have revealed that the regulatory repertoire present in multicellular animals 53 largely evolved first in a unicellular ancestor ( Fig. 1a) 2,5,6 . These insights contrast with a 54 widely-held view that all animals evolved from a stem organism that was a simple ball 55 of ciliated cells 1,3,4 . Implicit in this traditional perspective is that (i) regulatory systems 56 necessary for cell differentiation evolved after the divergence of metazoan and 57 choanoflagellates lineages, and (ii) morphological features shared between 58 choanoflagellate and choanocytes are homologous and were present in the original 59 animal cell. While the former is not supported by recent data -unicellular holozoans 60 can change cell states by environmentally-induced temporal shifts in gene expression 61 ( Fig. 1a) 5,6,10-12 -the latter is contingent upon the still controversial aspect of whether 62 extant choanocytes and choanoflagellates accurately reflect the ancestral animal cell 63 type. 64To test this, we first compared cell type-specific transcriptomes 13 from the sponge 65Amphimedon queenslandica with each other, and with transcriptomes expressed during 66 the life cycles of closely-related unicellular holozoans, the choanoflagellate Salpingoeca 67 rosetta, the filasterean Capsaspora owczarzaki and the ichthyosporean Creolimax 68 fragrantissima (Fig. 1a) 10-12 . We chose three sponge somatic cell types hypothesised to 69 be homologous to cells present in the last common ancestor of contemporary Extended Data Figure 2: Percentage of KEGG cellular processes and 663 environmental information processing (i.e. cell signalling) genes present in each 664 cell type, corresponding to the number of components making up each KEGG 665 category identified. 666 a, Cellular processes genes. b, Environmental information processing (i.e. cell 667 signalling) genes. 668 669 Extended Data Figure 3: Evolutionary age of genes expressed in Amphimedon 670 queenslandica choanocytes, archeocytes and pinacocytes using different 671 expression thresholds. 672 *
Marine pelagic larvae use a hierarchy of environmental cues to identify a suitable benthic habitat on which to settle and metamorphose into the adult phase of the life cycle. Most larvae are induced to settle by biochemical cues and many species have long been known to preferentially settle in the dark. Combined, these data suggest that larval responses to light and biochemical cues may be linked, but this has yet to be explored at the molecular level. Here, we track the vertical position of larvae of the sponge Amphimedon queenslandica to show that they descend to the benthos at twilight, by which time they are competent to respond to biochemical cues, consistent with them naturally settling in the dark. We use larval settlement assays under three different light regimes, combined with transcriptomics on individual larvae, to identify candidate molecular pathways underlying larval settlement. We find that larvae do not settle in response to biochemical cues if maintained in constant light. Our transcriptome data suggest that constant light actively represses settlement via the sustained up‐regulation of two putative inactivators of chemotransduction in constant light only. Our data suggest that photo‐ and chemosensory systems interact to regulate larval settlement via nitric oxide and cyclic guanosine monophosphate signalling in this sponge, which belongs to one of the earliest‐branching animal phyla.
Marine pelagic larvae use a hierarchy of environmental cues to identify a suitable benthic habitat on which to settle and metamorphose into the adult phase of the life cycle. Most larvae are induced to settle by biochemical cues and many species have long been known to preferentially settle in the dark. Combined, these data suggest that larval responses to light and biochemical cues may be linked, but this has yet to be explored at the molecular level. Here, we track the vertical position of larvae of the sponge Amphimedon queenslandica to show that they descend to the benthos at twilight, by which time they are competent to respond to biochemical cues, consistent with them naturally settling in the dark. We use larval settlement assays under three different light regimes, combined with transcriptomics on individual larvae, to identify candidate molecular pathways underlying larval settlement. We find that larvae do not settle in response to biochemical cues if maintained in constant light. Our transcriptome data suggest that constant light actively represses settlement via the sustained up‐regulation of two putative inactivators of chemotransduction in constant light only. Our data suggest that photo‐ and chemosensory systems interact to regulate larval settlement via nitric oxide and cyclic guanosine monophosphate signalling in this sponge, which belongs to one of the earliest‐branching animal phyla.
I acknowledge that an electronic copy of my thesis must be lodged with the University Library and, subject to the policy and procedures of The University of Queensland, the thesis be made available for research and study in accordance with the Copyright Act 1968 unless a period of embargo has been approved by the Dean of the Graduate School.
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