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Schierwater, B.

Publications and source records attributed to Schierwater, B..

4 recordsLinked to original sources

Evolution of the ribbon-like organization of the Golgi apparatus in animal cells

The Golgi ribbon is a structural organization formed by linked Golgi stacks that is believed to be exclusive to vertebrate cells. Its functional contribution to cellular processes is unclear, yet its disruption is associated with several human pathologies. In this study we address the evolutionary origin of the Golgi ribbon, describe a potential molecular mechanism for its emergence and identify a cellular process in which it may be involved. We observed the ribbon-like architecture in the cells of several metazoan taxa, suggesting its early appearance during animal evolution before the emergence of vertebrates. Supported by AlphaFold2 modelling, we propose that the evolution of the complex between two Golgi resident proteins, Golgin-45 and GRASP, led to the tethering of Golgi stacks into the ribbon-like configuration. Finally, we find that the ribbon is assembled during the early embryogenesis of deuterostome animals, a strong indication of its role in development. Overall, our study indicates that the Golgi ribbon is functionally relevant beyond vertebrates and calls for further investigations to decipher its elusive functions. O_FIG O_LINKSMALLFIG WIDTH=89 HEIGHT=200 SRC="FIGDIR/small/528797v2_ufig1.gif" ALT="Figure 1"> View larger version (33K): org.highwire.dtl.DTLVardef@17a404forg.highwire.dtl.DTLVardef@11413b4org.highwire.dtl.DTLVardef@119c036org.highwire.dtl.DTLVardef@19a512f_HPS_FORMAT_FIGEXP M_FIG Graphical abstract C_FIG

cell biology↗

Pleiotropy of Bcl-2 family proteins is an ancient trait in the metazoan evolution

In the animal kingdom, proteins of the Bcl-2 family are widely recognized as regulators of mitochondrial outer membrane permeabilization (MOMP), leading to apoptotic cell death. These proteins were recently also shown to control IP3-dependent calcium fluxes at the level of the endoplasmic reticulum (ER). However, the origin and evolution of these pleiotropic functions remain elusive. Here, we molecularly characterized the four members of the Bcl-2 family (trBcl-2L1 to -2L4) in the most primitive metazoan, namely Trichoplax adhaerens. Primary structure and phylogenetic analyses demonstrated that all four trBcl-2 homologs belong to the multidomain Bcl-2 group and presented a conserved C-terminus transmembrane (TM) domain. TrBcl-2L1 and trBcl-2L2 are highly divergent proteins clustering with the anti-apoptotic Bcl-2 members, whereas trBcl-2L3 and trBcl-2L4 were homologous to the pro-apoptotic Bax (trBax) and Bak (trBak). Interestingly, at the functional level, trBak operates as a BH3 only sensitizer repressing the anti-apoptotic activities of trBcl-2L1 and trBcl-2L2, whereas trBax leads to MOMP, similarly to the well-known indirect model of Bax activation. Finally, we found that trBcl-2L1 had a dual ER and mitochondrial subcellular localization and was able to bind to IP3R. By generating two TM domain mutants we demonstrated that trBcl-2L1 targeted to the ER was able to control IP3-dependent calcium fluxes, whereas Mito-trBcl-2L1 represses trBax-dependent MOMP, suggesting that Bcl-2 pleiotropy appeared early and was conserved throughout metazoan evolution.

evolutionary biology↗

High cell diversity and complex peptidergic signalling underlie placozoan behaviour

Placozoans, together with sponges, are the only animals devoid of a nervous system and muscles, yet both respond to sensory stimulation in a coordinated manner. How behavioural control in these free-living animals is achieved in the absence of neurons and, more fundamentally, how the first neurons evolved from more primitive communication cells during the rise of animals is not yet understood [1-5]. The placozoan Trichoplax adhaerens is a millimeter-wide, flat, free-living marine animal composed of six morphologically identified cell types distributed across a simple bodyplan [6-9]: a flat upper epithelium and a cylindrical lower epithelium interspersed with a loose layer of fiber cells. Its genome encodes several proneuropeptide genes and genes involved in neurosecretion in animals with a nervous system [10-12]. Here we investigate neuropeptide signalling in Trichoplax adhaerens. We found specific expression of several neuropeptides in non-overlapping cell populations distributed over the three cell layers, revealing an unsuspected cell-type diversity of Trichoplax adhaerens. Using live imaging, we uncovered that treatments with 11 different neuropeptides elicited striking and consistent effects on the animals shape, patterns of movement and velocity that we categorized under three main types: (i) crinkling, (ii) turning, and (iii) flattening and churning. Together, the data demonstrate a crucial role for peptidergic signalling in nerveless placozoans and suggest that peptidergic volume signalling may have predated synaptic signalling in the evolution of nervous systems.

neuroscience↗

A taxogenomics approach uncovers a new genus in the phylum Placozoa

The Placozoa [1] is a monotypic phylum of non-bilaterian marine animals. Its only species, Trichoplax adhaerens, was described in 1883 [2], Despite the worldwide distribution of placozoans [3-6], morphological differences are lacking among isolates from different geographic areas and, consequently, no other species in this phylum has been described and accepted for more than 130 years. However, recent single-gene studies on the genetic diversity of this \"species\" have revealed deeply divergent lineages of, as yet, undefined taxonomic ranks [3,5,6], Since single genes are not considered sufficient to define species [7], a whole nuclear genome comparison appears the most appropriate approach to determine relationships between placozoan lineages. Such a \"taxogenomics\" approach can help discover and diagnose potential additional species and, therefore, develop a much-needed, more robust, taxonomic framework for this phylum. To achieve this we sequenced the genome of a placozoan lineage isolated from Hong Kong (lineage H13), which is distantly related to T. adhaerens [6]. The 87 megabase genome assembly contains 12,010 genes. Comparison to the T. adhaerens genome [8] identified an average protein distance of 24.4% in more than 2,700 screened one-to-one orthologs, similar to levels observed between the chordate classes mammals and birds. Genome rearrangements are commonplace and >25% of genes are not collinear (i.e. they are not in the same order in the two genomes). Finally, a multi-gene distance comparison with other non-bilaterian phyla indicate genus level differences to T. adhaerens. These data highlight the large genomic diversity within the Placozoa and justifies the designation of lineage HI3 as a new species, Xxxxxxxxx yyyyyyyyyyyyy1 gen. et spaec. nov., now the second described placozoan species and the first in a new genus. Phylogenomic analyses furthermore supports a robust placement of the Placozoa as sister to a cnidarian-bilaterian clade.

evolutionary biology↗