Origins and Evolution of the α-L-Fucosidases: From Bacteria to Metazoans.
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ABSTRACT:
SUBMITTER: You J
PROVIDER: S-EPMC6718869 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Fucosylated carbohydrates and glycoproteins from human breast milk are essential for the development of the gut microbiota in early life because they are selectively metabolized by bifidobacteria. In this regard, α-L-fucosidases play a key role in this successful bifidobacterial colonization allowing the utilization of these substrates. Although a considerable number of α-L-fucosidases from bifidobacteria have been identified by computational analysis, only a few of them have been characterized. Hitherto, α-L-fucosidases are classified into three families: GH29, GH95, and GH151, based on their catalytic structure. However, bifidobacterial α-L-fucosidases belonging to a particular family show significant differences in their sequence. Because this fact could underlie distinct phylogenetic evolution, here extensive similarity searches and comparative analyses of the bifidobacterial α-L-fucosidases identified were carried out with the assistance of previous physicochemical studies available. This work reveals four and two paralogue bifidobacterial fucosidase groups within GH29 and GH95 families, respectively. Moreover, Bifidobacterium longum subsp. infantis species exhibited the greatest number of phylogenetic lineages in their fucosidases clustered in every family: GH29, GH95, and GH151. Since α-L-fucosidases phylogenetically descended from other glycosyl hydrolase families, we hypothesized that they could exhibit additional glycosidase activities other than fucosidase, raising the possibility of their application to transfucosylate substrates other than lactose in order to synthesis novel prebiotics.
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Project description:BackgroundBasal metabolic rate (BMR) has a very strong body-mass (M) dependence in an individual animal group, and BMR per unit mass (msBMR) converges on a markedly narrow range even across major taxonomic groups. However, it is here a basic question in metazoan biology how much BMR per unit mitochondrion (mtBMR) changes, and then whether mtBMR can be related to the original molecular mechanism of action of mt-encoded membrane proteins (MMPs) playing a central role in cellular energy production.Methodology/principal findingsAnalyzing variations of amino-acid compositions of MMPs across 13 metazoan animal groups, incorporating 2022 sequences, we found a strong inverse correlation between Ser/Thr composition (STC) and hydrophobicity (HYD). A majority of animal groups showed an evolutionary pathway of a gradual increase in HYD and decrease in STC, whereas only the deuterostome lineage revealed a rapid decrease in HYD and increase in STC. The strongest correlations appeared in 5 large subunits (ND4, ND5, ND2, CO1, and CO3) undergoing dynamic conformational changes for the proton-pumping function. The pathway of the majority groups is well understood as reflecting natural selection to reduce mtBMR, since simply raising HYD in MMPs (surrounded by the lipid bilayer) weakens their mobility and strengthens their stability. On the other hand, the marked decrease in HYD of the deuterostome elevates mtBMR, but is accompanied with their instability heightening a turnover rate of mitochondria and then cells. Interestingly, cooperative networks of interhelical hydrogen-bonds between motifs involving Ser and Thr residues can enhance MMP stability.Conclusion/significanceThis stability enhancement lowers turnover rates of mitochondria/cells and may prolong even longevity, and was indeed founded by strong positive correlations of STC with both mtBMR and longevity. The lowest HYD and highest STC in Aves and Mammals are congruent with their very high mtBMR and long longevity.
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Project description:CRISPR/Cas systems provide adaptive defense mechanisms against invading nucleic acids in prokaryotes. Because of its interest as a genetic tool, the Type II CRISPR/Cas9 system from Streptococcus pyogenes has been extensively studied. It includes the Cas9 endonuclease that is dependent on a dual-guide RNA made of a tracrRNA and a crRNA. Target recognition relies on crRNA annealing and the presence of a protospacer adjacent motif (PAM). Mollicutes are currently the bacteria with the smallest genome in which CRISPR/Cas systems have been reported. Many of them are pathogenic to humans and animals (mycoplasmas and ureaplasmas) or plants (phytoplasmas and some spiroplasmas). A global survey was conducted to identify and compare CRISPR/Cas systems found in the genome of these minimal bacteria. Complete or degraded systems classified as Type II-A and less frequently as Type II-C were found in the genome of 21 out of 52 representative mollicutes species. Phylogenetic reconstructions predicted a common origin of all CRISPR/Cas systems of mycoplasmas and at least two origins were suggested for spiroplasmas systems. Cas9 in mollicutes were structurally related to the S. aureus Cas9 except the PI domain involved in the interaction with the PAM, suggesting various PAM might be recognized by Cas9 of different mollicutes. Structure of the predicted crRNA/tracrRNA hybrids was conserved and showed typical stem-loop structures pairing the Direct Repeat part of crRNAs with the 5' region of tracrRNAs. Most mollicutes crRNA/tracrRNAs showed G + C% significantly higher than the genome, suggesting a selective pressure for maintaining stability of these secondary structures. Examples of CRISPR spacers matching with mollicutes phages were found, including the textbook case of Mycoplasma cynos strain C142 having no prophage sequence but a CRISPR/Cas system with spacers targeting prophage sequences that were found in the genome of another M. cynos strain that is devoid of a CRISPR system. Despite their small genome size, mollicutes have maintained protective means against invading DNAs, including restriction/modification and CRISPR/Cas systems. The apparent lack of CRISPR/Cas systems in several groups of species including main pathogens of humans, ruminants, and plants suggests different evolutionary routes or a lower risk of phage infection in specific ecological niches.
| S-EPMC6882279 | biostudies-literature
Project description:Bifidobacterium longum subsp. infantis ATCC 15697 utilizes several small-mass neutral human milk oligosaccharides (HMOs), several of which are fucosylated. Whereas previous studies focused on endpoint consumption, a temporal glycan consumption profile revealed a time-dependent effect. Specifically, among preferred HMOs, tetraose was favored early in fermentation, with other oligosaccharides consumed slightly later. In order to utilize fucosylated oligosaccharides, ATCC 15697 possesses several fucosidases, implicating GH29 and GH95 α-L-fucosidases in a gene cluster dedicated to HMO metabolism. Evaluation of the biochemical kinetics demonstrated that ATCC 15697 expresses three fucosidases with a high turnover rate. Moreover, several ATCC 15697 fucosidases are active on the linkages inherent to the HMO molecule. Finally, the HMO cluster GH29 α-L-fucosidase possesses a crystal structure that is similar to previously characterized fucosidases.
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Project description:Ezrin, radixin, moesin, and merlin are cytoskeletal proteins, whose functions are specific to metazoans. They participate in cell cortex rearrangement, including cell-cell contact formation, and play an important role in cancer progression. Here, we have performed a comprehensive phylogenetic analysis of the proteins spanning 87 species. The results describe a possible mechanism for the protein family origin in the root of Metazoa, paralogs diversification in vertebrates, and acquisition of novel functions, including tumor suppression. In addition, a merlin paralog, present in most vertebrates but lost in mammals, has been described here for the first time. We have also highlighted a set of amino acid variations within the conserved motifs as the candidates for determining physiological differences between ERM paralogs.
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Project description:BACKGROUND:One of the hallmarks of multicellular organisms is the ability of their cells to trigger responses to the environment in a coordinated manner. In recent years primary cilia have been shown to be present as 'antennae' on almost all animal cells, and are involved in cell-to-cell signaling in development and tissue homeostasis; how this sophisticated sensory system arose has been little-studied and its evolution is key to understanding how sensation arose in the Animal Kingdom. Sponges (Porifera), one of the earliest evolving phyla, lack conventional muscles and nerves and yet sense and respond to changes in their fluid environment. Here we demonstrate the presence of non-motile cilia in sponges and studied their role as flow sensors. RESULTS:Demosponges excrete wastes from their body with a stereotypic series of whole-body contractions using a structure called the osculum to regulate the water-flow through the body. In this study we show that short cilia line the inner epithelium of the sponge osculum. Ultrastructure of the cilia shows an absence of a central pair of microtubules and high speed imaging shows they are non-motile, suggesting they are not involved in generating flow. In other animals non-motile, 'primary', cilia are involved in sensation. Here we show that molecules known to block cationic ion channels in primary cilia and which inhibit sensory function in other organisms reduce or eliminate sponge contractions. Removal of the cilia using chloral hydrate, or removal of the whole osculum, also stops the contractions; in all instances the effect is reversible, suggesting that the cilia are involved in sensation. An analysis of sponge transcriptomes shows the presence of several transient receptor potential (TRP) channels including PKD channels known to be involved in sensing changes in flow in other animals. Together these data suggest that cilia in sponge oscula are involved in flow sensation and coordination of simple behaviour. CONCLUSIONS:This is the first evidence of arrays of non-motile cilia in sponge oscula. Our findings provide support for the hypothesis that the cilia are sensory, and if true, the osculum may be considered a sensory organ that is used to coordinate whole animal responses in sponges. Arrays of primary cilia like these could represent the first step in the evolution of sensory and coordination systems in metazoans.
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Project description:Several studies on 5S ribosomal DNA (5S rDNA) have been focused on a subset of the following features in mostly one organism: number of copies, pseudogenes, secondary structure, promoter and terminator characteristics, genomic arrangements, types of non-transcribed spacers and evolution. In this work, we systematically analyzed 5S rDNA sequence diversity in available metazoan genomes, and showed organism-specific and evolutionary-conserved features. Putatively functional sequences (12,766) from 97 organisms allowed us to identify general features of this multigene family in animals. Interestingly, we show that each mammal species has a highly conserved (housekeeping) 5S rRNA type and many variable ones. The genomic organization of 5S rDNA is still under debate. Here, we report the occurrence of several paralog 5S rRNA sequences in 58 of the examined species, and a flexible genome organization of 5S rDNA in animals. We found heterogeneous 5S rDNA clusters in several species, supporting the hypothesis of an exchange of 5S rDNA from one locus to another. A rather high degree of variation of upstream, internal and downstream putative regulatory regions appears to characterize metazoan 5S rDNA. We systematically studied the internal promoters and described three different types of termination signals, as well as variable distances between the coding region and the typical termination signal. Finally, we present a statistical method for detection of linkage among noncoding RNA (ncRNA) gene families. This method showed no evolutionary-conserved linkage among 5S rDNAs and any other ncRNA genes within Metazoa, even though we found 5S rDNA to be linked to various ncRNAs in several clades.
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Project description:Three putative α-L-fucosidases encoded in the Lactobacillus casei BL23 genome were cloned and purified. The proteins displayed different abilities to hydrolyze natural fucosyloligosaccharides like 2'-fucosyllactose, H antigen disaccharide, H antigen type II trisaccharide, and 3'-, 4'-, and 6'-fucosyl-GlcNAc. This indicated a possible role in the utilization of oligosaccharides present in human milk and intestinal mucosa.
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Project description:The dramatic increase in membrane proteome complexity is arguably one of the most pivotal evolutionary events that underpins the origin of multicellular animals. However, the origin of a significant number of membrane families involved in metazoan development has not been clarified. In this study, we have manually curated the membrane proteomes of 22 metazoan and 2 unicellular holozoan species. We identify 123,014 membrane proteins in these 24 eukaryotic species and classify 86% of the dataset. We determine 604 functional clusters that are present from the last holozoan common ancestor (LHCA) through many metazoan species. Intriguingly, we show that more than 70% of the metazoan membrane protein families have a premetazoan origin. The data show that enzymes are more highly represented in the LHCA and expand less than threefold throughout metazoan species; in contrast to receptors that are relatively few in the LHCA but expand nearly eight fold within metazoans. Expansions related to cell adhesion, communication, immune defence, and developmental processes are shown in conjunction with emerging biological systems, such as neuronal development, cytoskeleton organization, and the adaptive immune response. This study defines the possible LHCA membrane proteome and describes the fundamental functional clusters that underlie metazoan diversity and innovation.
| S-EPMC5620054 | biostudies-literature
Project description:Nature contains a tremendous diversity of forms both at the organismal and genomic levels. This diversity motivates the twin central questions of molecular evolution: what are the molecular mechanisms of adaptation, and what are the functional consequences of genomic diversity. We report a 22-species comparative analysis of tropomyosin (PPM) genes, which exist in a variety of forms and are implicated in the emergence of a wealth of cellular functions, including the novel muscle functions integral to the functional diversification of bilateral animals. TPM genes encode either or both of long-form [284 amino acid (aa)] and short-form (approximately 248 aa) proteins. Consistent with a role of TPM diversification in the origins and radiation of bilaterians, we find evidence that the muscle-specific long-form protein arose in proximal bilaterian ancestors (the bilaterian 'stem'). Duplication of the 5' end of the gene led to alternative promoters encoding long- and short-form transcripts with distinct functions. This dual-function gene then underwent strikingly parallel evolution in different bilaterian lineages. In each case, recurrent tandem exon duplication and mutually exclusive alternative splicing of the duplicates, with further association between these alternatively spliced exons along the gene, led to long- and short-form-specific exons, allowing for gradual emergence of alternative "internal paralogs" within the same gene. We term these Mutually exclusively Alternatively spliced Tandemly duplicated Exon sets "MATEs". This emergence of internal paralogs in various bilaterians has employed every single TPM exon in at least one lineage and reaches striking levels of divergence with up to 77% of long- and short-form transcripts being transcribed from different genomic regions. Interestingly, in some lineages, these internal alternatively spliced paralogs have subsequently been "externalized" by full gene duplication and reciprocal retention/loss of the two transcript isoforms, a particularly clear case of evolution by subfunctionalization. This parallel evolution of TPM genes in diverse metazoans attests to common selective forces driving divergence of different gene transcripts and represents a striking case of emergence of evolutionary novelty by alternative splicing.
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