The origin of multicellularity in cyanobacteria

Schirrmeister, Bettina E.; Antonelli, Alexandre; Bagheri, Homayoun C.

doi:10.1186/1471-2148-11-45

Cited by 251 publications

(233 citation statements)

References 109 publications

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“…19, 21, and 24). This rooting, however, is sensitive to the choice of out-group species (25). In contrast to these results, we find Gloeobacter violaceus emerging relatively late (node 16 in Fig.…”

contrasting

confidence: 55%

Phylogenetic modeling of lateral gene transfer reconstructs the pattern and relative timing of speciations

Szöllősi

Boussau

Abby

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

155

187

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The timing of the evolution of microbial life has largely remained elusive due to the scarcity of prokaryotic fossil record and the confounding effects of the exchange of genes among possibly distant species. The history of gene transfer events, however, is not a series of individual oddities; it records which lineages were concurrent and thus provides information on the timing of species diversification. Here, we use a probabilistic model of genome evolution that accounts for differences between gene phylogenies and the species tree as series of duplication, transfer, and loss events to reconstruct chronologically ordered species phylogenies. Using simulations we show that we can robustly recover accurate chronologically ordered species phylogenies in the presence of gene tree reconstruction errors and realistic rates of duplication, transfer, and loss. Using genomic data we demonstrate that we can infer rooted species phylogenies using homologous gene families from complete genomes of 10 bacterial and archaeal groups. Focusing on cyanobacteria, distinguished among prokaryotes by a relative abundance of fossils, we infer the maximum likelihood chronologically ordered species phylogeny based on 36 genomes with 8,332 homologous gene families. We find the order of speciation events to be in full agreement with the fossil record and the inferred phylogeny of cyanobacteria to be consistent with the phylogeny recovered from established phylogenomics methods. Our results demonstrate that lateral gene transfers, detected by probabilistic models of genome evolution, can be used as a source of information on the timing of evolution, providing a valuable complement to the limited prokaryotic fossil record. molecular dating | gene tree reconciliation | birth-death model A central aspect of Earth's history is the pattern and timing of diversification of the species that inhabit it. In macroorganisms such as animals or plants, an abundant fossil record, the accumulation of genomic data, and the development of models of molecular evolution accommodating for varying rates of evolutionary changes among lineages are progressively yielding an intelligible picture (1-4). In contrast, the dating of the evolution of microbial life remains largely elusive (5, 6). This situation results from the convergence of two main factors: first, fossils, especially bacterial and archaeal ones, are scarce or cannot be traced to a specific lineage. Therefore, any inference of the timing of microbial evolution must rely almost exclusively on molecular data constrained only by a handful of dates during the course of more than three billion years of evolution. Second, molecular data can be difficult to interpret in terms of patterns of species diversification. Lateral gene transfers (LGTs), the exchange of genes among possibly distant species, have tangled gene phylogenies to the extent that they provide a deeply blurred view of the relationships between lineages. Different approaches [e.g., concatenation, supertrees (7, 8)] have been proposed to ove...

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contrasting

confidence: 55%

Phylogenetic modeling of lateral gene transfer reconstructs the pattern and relative timing of speciations

Szöllősi

Boussau

Abby

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

155

187

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“…15) gave rise to chloroplasts. However, this classification is mainly based on morphology, and recent phylogenetic studies 12 have shown that morphological characters are poor indicators of relatedness in cyanobacteria. Hence, doubt still remains concerning the exact origin of chloroplasts, and the release of more cyanobacterial genome sequences may alter our understanding of the origin of the Toc75 and OEP80 families.…”

Section: Phylogenetic Analysis Of Toc75 and Oep80 Proteinsmentioning

confidence: 99%

“…To root our tree, we used a sequence from Gloeobacter violaceus, which is hypothesized to form the sister group of all other cyanobacteria. 12,13 Doing this (in addition to an extensive reciprocal search for homologs among cyanobacterial sequences) showed that all eukaryotic representatives of the Toc75 and OEP80 clades probably have a single common origin in prokaryotes. Uncertainty in this regard largely derives from a lack of information on the identity of the cyanobacterial group from which chloroplasts originate.…”

Section: Phylogenetic Analysis Of Toc75 and Oep80 Proteinsmentioning

confidence: 99%

Neofunctionalization within the Omp85 protein superfamily during chloroplast evolution

Töpel

Ling

Jarvis

2012

Plant Signaling & Behavior

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The Toc75 and OEP80 proteins reside in the chloroplast outer envelope membrane. Both are members of the Omp85 superfamily of b-barrel proteins, and both are essential in Arabidopsis plants with important roles throughout development. Toc75 forms the translocation channel of the TOC complex, which is responsible for importing nucleus-encoded proteins into chloroplasts, while the function of OEP80 remains uncertain. Deficiency of Toc75 in plants that have artificially reduced OEP80 levels suggests that the latter may be involved in the biogenesis of b-barrel proteins, in similar fashion to Omp85-related proteins in other systems. To elucidate the evolutionary relationship between the two proteins, we conducted a phylogenetic analysis using 48 sequences from diverse species. This indicated that Toc75 and OEP80 belong to sister groups in the Omp85 superfamily, and originate from a gene duplication in an ancient eukaryotic organism . 1.2 billion years ago. Our analysis also supports the notion that the Toc75 family has undergone a phase of neofunctionalization to accommodate the organelle's newly acquired need to import proteins. Chloroplasts, Protein Import, and Omp85-Related ProteinsChloroplasts evolved through endosymbiosis from an ancient relative of extant cyanobacteria approximately 1.5 billion years ago.1 Ensuing organellar genome reduction and the transfer of genetic material to the nucleus together led to the need for modern chloroplasts to import . 90% of the 3,000 or so different proteins that are required for organellar functions. This import process is mediated by multiprotein complexes in the double membrane surrounding each organelle, termed TOC and TIC (translocon at the outer/inner envelope membrane of chloroplasts). 2The β-barrel protein Toc75 is a core component of the TOC complex and it forms the main translocation channel in the outer membrane. Furthermore, Toc75 is a member of a ubiquitous family of proteins that all possess a similar structure, which together are often referred to as the Omp85 (or BamA) superfamily.3,4 Other family members include Omp85, which mediates outer membrane protein biogenesis in Gram-negative bacteria, and Sam50/Tob55, which performs a similar role in mitochondria. Interestingly, in chloroplasts there is a second Omp85 family member called OEP80 (outer envelope protein of 80 kDa; or Toc75-V, the Roman numeral being a reference to the chromosomal location of the gene in Arabidopsis). The role of OEP80 is uncertain, although functional analogy with bacterial Omp85 and mitochondrial Sam50/Tob55 has been proposed.In Arabidopsis, the only full-length Toc75 and OEP80 genes (i.e., atTOC75-III and AtOEP80, respectively) are essential, with knockout mutants causing embryo abortion. 5,6 The lethality of the knockout mutations limits their use in relation to functional in vivo analyses, and so in a recent study inducible RNA interference (RNAi) was used to knockdown expression of the genes during postembryonic growth.7 This revealed the importance of both genes during later stag...

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“…Numbers at the nodes represent the posterior probability. The grouping of cyanobacteria is according to Schirrmeister et al, 2011. Cyanobacteria marked with an asterisk (Gloeobacter violaceus PCC 7421 and Cyanobacterium UCYN-A) are devoid of the Rps1b homolog.…”

Section: High Incidence Of Short Cis-encoded Asrnasmentioning

confidence: 99%

Comparative transcriptomics of two environmentally relevant cyanobacteria reveals unexpected transcriptome diversity

et al. 2014

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Prochlorococcus is a genus of abundant and ecologically important marine cyanobacteria. Here, we present a comprehensive comparison of the structure and composition of the transcriptomes of two Prochlorococcus strains, which, despite their similarities, have adapted their gene pool to specific environmental constraints. We present genome-wide maps of transcriptional start sites (TSS) for both organisms, which are representatives of the two most diverse clades within the two major ecotypes adapted to high-and low-light conditions, respectively. Our data suggest antisense transcription for three-quarters of all genes, which is substantially more than that observed in other bacteria. We discovered hundreds of TSS within genes, most notably within 16 of the 29 prochlorosin genes, in strain MIT9313. A direct comparison revealed very little conservation in the location of TSS and the nature of non-coding transcripts between both strains. We detected extremely short 5 0 untranslated regions with a median length of only 27 and 29 nt for MED4 and MIT9313, respectively, and for 8% of all protein-coding genes the median distance to the start codon is only 10 nt or even shorter. These findings and the absence of an obvious Shine-Dalgarno motif suggest that leaderless translation and ribosomal protein S1-dependent translation constitute alternative mechanisms for translation initiation in Prochlorococcus. We conclude that genomewide antisense transcription is a major component of the transcriptional output from these relatively small genomes and that a hitherto unrecognized high degree of complexity and variability of gene expression exists in their transcriptional architecture.

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The origin of multicellularity in cyanobacteria

Cited by 251 publications

References 109 publications

Phylogenetic modeling of lateral gene transfer reconstructs the pattern and relative timing of speciations

Phylogenetic modeling of lateral gene transfer reconstructs the pattern and relative timing of speciations

Neofunctionalization within the Omp85 protein superfamily during chloroplast evolution

Comparative transcriptomics of two environmentally relevant cyanobacteria reveals unexpected transcriptome diversity

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