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Sterols in a unicellular relative of the metazoans.

ABSTRACT: Molecular clocks suggest that animals originated well before they first appear as macroscopic fossils, but geologic tests of these hypotheses have been elusive. A rare steroid hydrocarbon, 24-isopropylcholestane, has been hypothesized to be a biomarker for sponges or their immediate ancestors because of its relatively high abundance in pre-Ediacaran to Early Cambrian sedimentary rocks and oils. Biolipid precursors of this sterane have been reported to be prominent in several demosponges. Whether 24-isopropylcholestane can be interpreted as a sponge (and, hence, animal) biomarker, and so provide clues about early metazoan history, depends on an understanding of the distribution of sterol biosynthesis among animals and their protistan relatives. Accordingly, we characterized the sterol profile of the choanoflagellate Monosiga brevicollis, a representative of the unicellular sister group of animals. M. brevicollis does not produce a candidate sterol precursor for 24-isopropylcholestane under our experimental growth conditions. It does, however, produce a number of other sterols, and comparative genomics confirms its biosynthetic potential to produce the full suite of compounds recovered. Consistent with the phylogenetic position of choanoflagellates, the sterol profile and biosynthetic pathway of M. brevicollis display characteristics of both fungal and poriferan sterol biosynthesis. This is an example in which genomic and biochemical information have been used together to investigate the taxonomic specificity of a fossil biomarker.

SUBMITTER: Kodner RB

PROVIDER: S-EPMC2481317 | biostudies-literature | 2008 Jul

REPOSITORIES: biostudies-literature

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Sterols in a unicellular relative of the metazoans.

Kodner Robin B RB Summons Roger E RE Pearson Ann A King Nicole N Knoll Andrew H AH

Proceedings of the National Academy of Sciences of the United States of America 20080715 29

Molecular clocks suggest that animals originated well before they first appear as macroscopic fossils, but geologic tests of these hypotheses have been elusive. A rare steroid hydrocarbon, 24-isopropylcholestane, has been hypothesized to be a biomarker for sponges or their immediate ancestors because of its relatively high abundance in pre-Ediacaran to Early Cambrian sedimentary rocks and oils. Biolipid precursors of this sterane have been reported to be prominent in several demosponges. Whether ...[more]

PMID: 18632573

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Project description:BackgroundComparative genomics of the early diverging metazoan lineages and of their unicellular sister-groups opens new window to reconstructing the genetic changes which preceded or accompanied the evolution of multicellular body plans. A recent analysis found that the genome of the nerve-less sponges encodes the homologues of most vertebrate post-synaptic proteins. In vertebrate excitatory synapses, these proteins assemble to form the post-synaptic density, a complex molecular platform linking membrane receptors, components of their signalling pathways, and the cytoskeleton. Newly available genomes from Monosiga brevicollis (a member of Choanoflagellata, the closest unicellular relatives of animals) and Trichoplax adhaerens (a member of Placozoa: besides sponges, the only nerve-less metazoans) offer an opportunity to refine our understanding of post-synaptic protein evolution.ResultsSearches for orthologous proteins and reconstruction of gene gains/losses based on the taxon phylogeny indicate that post-synaptic proteins originated in two main steps. The backbone scaffold proteins (Shank, Homer, DLG) and some of their partners were acquired in a unicellular ancestor of choanoflagellates and metazoans. A substantial additional set appeared in an exclusive ancestor of the Metazoa. The placozoan genome contains most post-synaptic genes but lacks some of them. Notably, the master-scaffold protein Shank might have been lost secondarily in the placozoan lineage.ConclusionsThe time of origination of most post-synaptic proteins was not concomitant with the acquisition of synapses or neural-like cells. The backbone of the scaffold emerged in a unicellular context and was probably not involved in cell-cell communication. Based on the reconstructed protein composition and potential interactions, its ancestral function could have been to link calcium signalling and cytoskeleton regulation. The complex later became integrated into the evolving synapse through the addition of novel functionalities.

Project description:Significant increases in sedimentation rate accompany the evolution of multicellularity. These increases should lead to rapid changes in ecological distribution, thereby affecting the costs and benefits of multicellularity and its likelihood to evolve. However, how genetic and cellular traits control this process, their likelihood of emergence over evolutionary timescales, and the variation in these traits as multicellularity evolves are still poorly understood. Here, using isolates of the ichthyosporean genus Sphaeroforma-close unicellular relatives of animals with brief transient multicellular life stages-we demonstrate that sedimentation rate is a highly variable and evolvable trait affected by at least 2 distinct physical mechanisms. First, we find extensive (>300×) variation in sedimentation rates for different Sphaeroforma species, mainly driven by size and density during the unicellular-to-multicellular life cycle transition. Second, using experimental evolution with sedimentation rate as a focal trait, we readily obtained, for the first time, fast settling and multicellular Sphaeroforma arctica isolates. Quantitative microscopy showed that increased sedimentation rates most often arose by incomplete cellular separation after cell division, leading to clonal "clumping" multicellular variants with increased size and density. Strikingly, density increases also arose by an acceleration of the nuclear doubling time relative to cell size. Similar size- and density-affecting phenotypes were observed in 4 additional species from the Sphaeroforma genus, suggesting that variation in these traits might be widespread in the marine habitat. By resequencing evolved isolates to high genomic coverage, we identified mutations in regulators of cytokinesis, plasma membrane remodeling, and chromatin condensation that may contribute to both clump formation and the increase in the nuclear number-to-volume ratio. Taken together, this study illustrates how extensive cellular control of density and size drive sedimentation rate variation, likely shaping the onset and further evolution of multicellularity.

Project description:The genomes of close unicellular relatives of animals encode orthologs of many genes that regulate animal development. However, little is known about the function of such genes in unicellular organisms or the evolutionary process by which these genes came to function in multicellular development. The Hippo pathway, which regulates cell proliferation and tissue size in animals, is present in some of the closest unicellular relatives of animals, including the amoeboid organism Capsaspora owczarzaki. We previously showed that the Capsaspora ortholog of the Hippo pathway nuclear effector Yorkie/YAP/TAZ (coYki) regulates actin dynamics and the three-dimensional morphology of Capsaspora cell aggregates, but is dispensable for cell proliferation control (Phillips et al., 2022). However, the function of upstream Hippo pathway components, and whether and how they regulate coYki in Capsaspora, remained unknown. Here, we analyze the function of the upstream Hippo pathway kinases coHpo and coWts in Capsaspora by generating mutant lines for each gene. Loss of either kinase results in increased nuclear localization of coYki, indicating an ancient, premetazoan origin of this Hippo pathway regulatory mechanism. Strikingly, we find that loss of either kinase causes a contractile cell behavior and increased density of cell packing within Capsaspora aggregates. We further show that this increased cell density is not due to differences in proliferation, but rather actomyosin-dependent changes in the multicellular architecture of aggregates. Given its well-established role in cell density-regulated proliferation in animals, the increased density of cell packing in coHpo and coWts mutants suggests a shared and possibly ancient and conserved function of the Hippo pathway in cell density control. Together, these results implicate cytoskeletal regulation but not proliferation as an ancestral function of the Hippo pathway kinase cascade and uncover a novel role for Hippo signaling in regulating cell density in a proliferation-independent manner.

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Sterols in a unicellular relative of the metazoans.

Publications

Sterols in a unicellular relative of the metazoans.

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