Emergence Of Metazoans Research Articles

Refining the early Cambrian marine redox profile by using pyrite sulfur and iron isotopes

It is widely accepted that the emergence of metazoans in the Ediacaran-Cambrian transition might be triggered by oxygenation of the atmosphere-ocean system. However, some Ediacaran and early Cambrian macroscopic fossils (such as multicellular algae) were preserved under sulfidic conditions, challenging the conventional view of the prohibition of eukaryotes in the presence of H2S. It was proposed that organisms might have lived in some episodic non-sulfidic intervals although the ocean was predominantly sulfidic. However, the hypothesized short-lived non-sulfidic intervals were hardly identified by traditional bulk sample analyses, which cannot provide sufficiently high temporal resolution to resolve the short-term oxygenation events. In this study, we analyzed pyritized sponge spicules and disseminated pyrites from black shales of the early Cambrian Shuijingtuo Formation in South China. We conducted in situ pyrite sulfur (δ34Spy) and iron (δ56Fepy) isotopes as well as bulk sample pyrite sulfur isotope analyses. The intra-crystal or intra-spicule δ34Spy variations reflect the evolution of seawater and porewater geochemistry during pyrite formation, providing a higher temporal resolution of redox fluctuation in the early Cambrian ocean. Our study indicates: (1) The bulk sample pyrite sulfur isotope and pyrite content data suggest diagenetic pyrite precipitation in sediment porewater with H2S diffusion from the overlying sulfidic seawater; (2) Limited intra-crystal and intra-spicule δ34Spy variations imply that both spicule and disseminate pyrites had a homogenous S source from sulfidic seawater, and dissimilatory sulfate reduction (DSR) in sediment porewater was negligible; (3) The in situ iron isotope analyses indicate active dissimilatory iron reduction (DIR) in sediment that generated excessive ferrous iron (Fe2+) to compensate for Fe2+ consumption by pyrite precipitation, allowing Fe2+ to accumulate in ferruginous porewater. Therefore, the early Cambrian ocean was characterized by active DSR in sulfidic seawater and DIR in ferruginous sediment porewater. In addition, our study demonstrates that the seawater might be persistently sulfidic, and does not support the presence of intermittent non-sulfidic intervals for the survival of organisms. If correct, it is hypothesized that some primitive sponges might have survived in sulfidic seawater, although the seawater H2S concentration remains unknown.

Ancient Origins of Cytoskeletal Crosstalk: Spectraplakin-like Proteins Precede the Emergence of Cortical Microtubule Stabilization Complexes as Crosslinkers.

Adhesion between cells and the extracellular matrix (ECM) is one of the prerequisites for multicellularity, motility, and tissue specialization. Focal adhesions (FAs) are defined as protein complexes that mediate signals from the ECM to major components of the cytoskeleton (microtubules, actin, and intermediate filaments), and their mutual communication determines a variety of cellular processes. In this study, human cytoskeletal crosstalk proteins were identified by comparing datasets with experimentally determined cytoskeletal proteins. The spectraplakin dystonin was the only protein found in all datasets. Other proteins (FAK, RAC1, septin 9, MISP, and ezrin) were detected at the intersections of FAs, microtubules, and actin cytoskeleton. Homology searches for human crosstalk proteins as queries were performed against a predefined dataset of proteomes. This analysis highlighted the importance of FA communication with the actin and microtubule cytoskeleton, as these crosstalk proteins exhibit the highest degree of evolutionary conservation. Finally, phylogenetic analyses elucidated the early evolutionary history of spectraplakins and cortical microtubule stabilization complexes (CMSCs) as model representatives of the human cytoskeletal crosstalk. While spectraplakins probably arose at the onset of opisthokont evolution, the crosstalk between FAs and microtubules is associated with the emergence of metazoans. The multiprotein complexes contributing to cytoskeletal crosstalk in animals gradually gained in complexity from the onset of metazoan evolution.

Mitochondria Are Fundamental for the Emergence of Metazoans: On Metabolism, Genomic Regulation, and the Birth of Complex Organisms.

Out of many intracellular bacteria, only the mitochondria and chloroplasts abandoned their independence billions of years ago and became endosymbionts within the host eukaryotic cell. Consequently, one cannot grow eukaryotic cells without their mitochondria, and the mitochondria cannot divide outside of the cell, thus reflecting interdependence. Here, we argue that such interdependence underlies the fundamental role of mitochondrial activities in the emergence of metazoans. Several lines of evidence support our hypothesis: (a) Differentiation and embryogenesis rely on mitochondrial function; (b) mitochondrial metabolites are primary precursors for epigenetic modifications (such as methyl and acetyl), which are critical for chromatin remodeling and gene expression, particularly during differentiation and embryogenesis; and (c) mitonuclear coregulation adapted to accommodate both housekeeping and tissue-dependent metabolic needs. We discuss the evolution of the unique mitochondrial genetic system, mitochondrial metabolites, mitonuclear coregulation, and their critical roles in the emergence of metazoans and in human disorders.

The Origin of Metazoa: An Algorithmic View of Life

We propose that the sudden emergence of metazoans during the Cambrian was due to the appearance of a complex genome architecture that was capable of computing. In turn, this made defining recursive functions possible. The underlying molecular changes that occurred in tandem were driven by the increased probability of maintaining duplicated DNA fragments in the metazoan genome. In our model, an increase in telomeric units, in conjunction with a telomerase-negative state and consequent telomere shortening, generated a reference point equivalent to a non-reversible counting mechanism.

Molecular Determinants for the Genesis of the Action Potential

In nerves and muscles, action potentials are initiated by the rapid activation of voltage-gated sodium (Nav) channels and terminated by the delayed activation of voltage-gated potassium (Kv) channels. This sequential activation, which is the prerequisite for the genesis of the action potential, requires faster activation kinetics of the voltage-sensor domains (VSD) in Nav as compared to Kv channels. Despite on decades of investigations, the molecular determinants and mechanisms underlying this phenomenon remain elusive. Here, we show that this differential gating is mostly imparted by six conserved hydrophilic residues Thr or Ser located in the S2 and S4 segments of the VSD in domains I-III of Nav channels while these positions are commonly occupied by hydrophobic residues in the VSD of Kv channels. Hydrophilic substitutions at the S2 position in the Shaker Kv channel accelerate the gating charge transfer by decreasing its energy barrier while hydrophilic substitutions at the S4 position speed up VSD activation by destabilizing its resting conformation. Interestingly, these hydrophilic residues are present in a Nav-related gene expressed in an evolutionary-distant unicellular choanoflagellate, suggesting that rapidly-gated Nav channels evolved before the emergence of metazoans and their nervous systems. We also show that the physiological co-expression of the ubiquitous regulatory β1 subunit further accelerates VSD movement in both a neuronal and a muscular Nav, providing a molecular basis for the β1-dependent fast gating mode previously detected from the ionic conductance. Our study uncovers the fundamental molecular determinants and possible mechanisms that enabled the differential gating in sodium and potassium channels and the emergence of the action potential. This work was supported by NIH grant GM030376.

Lack of Csk-Mediated Negative Regulation in a Unicellular Src Kinase

Phosphotyrosine-based signaling plays a vital role in cellular communication in multicellular organisms. Unexpectedly, unicellular choanoflagellates (the closest phylogenetic group to metazoans) possess numbers of tyrosine kinases that are comparable to those in complex metazoans. Here, we have characterized tyrosine kinases from the filasterean Capsaspora owczarzaki, a unicellular protist representing the sister group to choanoflagellates and metazoans. Two Src-like tyrosine kinases have been identified in C. owczarzaki (CoSrc1 and CoSrc2), both of which have the arrangement of SH3, SH2, and catalytic domains seen in mammalian Src kinases. In Capsaspora cells, CoSrc1 and CoSrc2 localize to punctate structures in filopodia that may represent primordial focal adhesions. We have cloned, expressed, and purified both enzymes. CoSrc1 and CoSrc2 are active tyrosine kinases. Mammalian Src kinases are normally regulated in a reciprocal fashion by autophosphorylation in the activation loop (which increases activity) and by Csk-mediated phosphorylation of the C-terminal tail (which inhibits activity). Similar to mammalian Src kinases, the enzymatic activities of CoSrc1 and CoSrc2 are increased by autophosphorylation in the activation loop. We have identified a Csk-like kinase (CoCsk) in the genome of C. owczarzaki. We cloned, expressed, and purified CoCsk and found that it has no measurable tyrosine kinase activity. Furthermore, CoCsk does not phosphorylate or regulate CoSrc1 or CoSrc2 in cells or in vitro, and CoSrc1 and CoSrc2 are active in Capsaspora cell lysates. Thus, the function of Csk as a negative regulator of Src family kinases appears to have arisen with the emergence of metazoans.

Did detoxification processes cause complex life to emerge?

Excess oxygen is toxic for many cells and cell function can be disrupted by calcium, even if present in small amounts. Cells avoid the toxic effects of these substances by excreting oxygen-rich or Ca-containing molecules. The origin of macroscopic multi-celled animals (metazoans) can be attributed to the excretion of oxygen-rich collagen molecules (or their precursors) at a time when the seas were for the first time both oxygenated and sufficiently loaded with phosphorus for the energy (ATP) requirements of sizable metazoans. With subsequent increase of Ca in the marine environment, hard parts of CaCO3 were produced. Excretion of oxygen in combination with abundant phosphorus permitted phosphate biomineralization. In this view, the most informative biological development during the late Neoproterozoic was not the emergence of metazoans but the initial construction of viable tissues. When tissue integrity is lost, whether due to low oxygen, collagen failure, injury, chemical insult or other reasons, individual cells are released from tissue-constraints. To survive, they may then revert to unicellular life-styles that emphasize cellular proliferation and variation. When this occurs in metazoans, the result may be cancer.

Origin of the paired domain.

Pax proteins play a diverse role in early animal development and contain the characteristic paired domain, consisting of two conserved helix-turn-helix motifs. In many Pax proteins the paired domain is fused to a second DNA binding domain of the paired-like homeobox family. By amino acid sequence alignments, secondary structure prediction, 3D-structure comparison, and phylogenetic reconstruction, we analyzed the relationship between Pax proteins and members of the Tc1 family of transposases, which possibly share a common ancestor with Pax proteins. We suggest that the DNA binding domain of an ancestral transposase (proto-Pax transposase) was fused to a homeodomain shortly after the emergence of metazoans about one billion years ago. Using the transposase sequences as an outgroup we reexamined the early evolution of the Pax proteins. Our novel evolutionary scenario features a single homeobox capturing event and an early duplication of Pax genes before the divergence of porifera, indicating a more diverse role of Pax proteins in primitive animals than previously expected.

Symbiotic emergence of metazoans.

IT has been assumed that differentiation during embryonic development is based on the regulation of gene activities. The differentiation of each cell, then, results from the activity of certain genes and the inactivity of others. Practically all theories of embryonic development rely on this assumption (see Markert1). It is evident that different genes are active in different cells (that is to say, haemoglobin genes in erythroblasts, thyroglobulin genes in thyroid cells, myosin genes in muscle cells). But the precise programming of cells containing thousands of genes still fails to explain the regular embryonic development, which depends not only on cellular differentiation but on precise cell divisions, cell and tissue movements, cell interactions and even cell death. Moreover, embryonic development is flexible enough to respond to injury, from the formation of complete identical twins to the fusion of two organs to form a single one.