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Flexibility and constraint: Evolutionary remodeling of the sporulation initiation pathway in Firmicutes.

ABSTRACT: The evolution of signal transduction pathways is constrained by the requirements of signal fidelity, yet flexibility is necessary to allow pathway remodeling in response to environmental challenges. A detailed understanding of how flexibility and constraint shape bacterial two component signaling systems is emerging, but how new signal transduction architectures arise remains unclear. Here, we investigate pathway remodeling using the Firmicute sporulation initiation (Spo0) pathway as a model. The present-day Spo0 pathways in Bacilli and Clostridia share common ancestry, but possess different architectures. In Clostridium acetobutylicum, sensor kinases directly phosphorylate Spo0A, the master regulator of sporulation. In Bacillus subtilis, Spo0A is activated via a four-protein phosphorelay. The current view favors an ancestral direct phosphorylation architecture, with the phosphorelay emerging in the Bacillar lineage. Our results reject this hypothesis. Our analysis of 84 broadly distributed Firmicute genomes predicts phosphorelays in numerous Clostridia, contrary to the expectation that the Spo0 phosphorelay is unique to Bacilli. Our experimental verification of a functional Spo0 phosphorelay encoded by Desulfotomaculum acetoxidans (Class Clostridia) further supports functional phosphorelays in Clostridia, which strongly suggests that the ancestral Spo0 pathway was a phosphorelay. Cross complementation assays between Bacillar and Clostridial phosphorelays demonstrate conservation of interaction specificity since their divergence over 2.7 BYA. Further, the distribution of direct phosphorylation Spo0 pathways is patchy, suggesting multiple, independent instances of remodeling from phosphorelay to direct phosphorylation. We provide evidence that these transitions are likely the result of changes in sporulation kinase specificity or acquisition of a sensor kinase with specificity for Spo0A, which is remarkably conserved in both architectures. We conclude that flexible encoding of interaction specificity, a phenotype that is only intermittently essential, and the recruitment of kinases to recognize novel environmental signals resulted in a consistent and repeated pattern of remodeling of the Spo0 pathway.

SUBMITTER: Davidson P

PROVIDER: S-EPMC6136694 | biostudies-literature | 2018 Sep

REPOSITORIES: biostudies-literature

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Flexibility and constraint: Evolutionary remodeling of the sporulation initiation pathway in Firmicutes.

Davidson Philip P Eutsey Rory R Redler Brendan B Hiller N Luisa NL Laub Michael T MT Durand Dannie D

PLoS genetics 20180913 9

The evolution of signal transduction pathways is constrained by the requirements of signal fidelity, yet flexibility is necessary to allow pathway remodeling in response to environmental challenges. A detailed understanding of how flexibility and constraint shape bacterial two component signaling systems is emerging, but how new signal transduction architectures arise remains unclear. Here, we investigate pathway remodeling using the Firmicute sporulation initiation (Spo0) pathway as a model. Th ...[more]

PMID: 30212463

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Project description:The current classification of the phylum Firmicutes (new name, Bacillota) features eight distinct classes, six of which include known spore-forming bacteria. In Bacillus subtilis, sporulation involves up to 500 genes, many of which do not have orthologs in other bacilli and/or clostridia. Previous studies identified about 60 sporulation genes of B. subtilis that were shared by all spore-forming members of the Firmicutes. These genes are referred to as the sporulation core or signature, although many of these are also found in genomes of nonsporeformers. Using an expanded set of 180 firmicute genomes from 160 genera, including 76 spore-forming species, we investigated the conservation of the sporulation genes, in particular seeking to identify lineages that lack some of the genes from the conserved sporulation core. The results of this analysis confirmed that many small acid-soluble spore proteins (SASPs), spore coat proteins, and germination proteins, which were previously characterized in bacilli, are missing in spore-forming members of Clostridia and other classes of Firmicutes. A particularly dramatic loss of sporulation genes was observed in the spore-forming members of the families Planococcaceae and Erysipelotrichaceae. Fifteen species from diverse lineages were found to carry skin (sigK-interrupting) elements of different sizes that all encoded SpoIVCA-like recombinases but did not share any other genes. Phylogenetic trees built from concatenated alignments of sporulation proteins and ribosomal proteins showed similar topology, indicating an early origin and subsequent vertical inheritance of the sporulation genes. IMPORTANCE Many members of the phylum Firmicutes (Bacillota) are capable of producing endospores, which enhance the survival of important Gram-positive pathogens that cause such diseases as anthrax, botulism, colitis, gas gangrene, and tetanus. We show that the core set of sporulation genes, defined previously through genome comparisons of several bacilli and clostridia, is conserved in a wide variety of sporeformers from several distinct lineages of Firmicutes. We also detected widespread loss of sporulation genes in many organisms, particularly within the families Planococcaceae and Erysipelotrichaceae. Members of these families, such as Lysinibacillus sphaericus and Clostridium innocuum, could be excellent model organisms for studying sporulation mechanisms, such as engulfment, formation of the spore coat, and spore germination.

Project description:BackgroundProteins play a key role in cellular life. They do not act alone but are organised in complexes. Throughout the life of a cell, complexes are dynamic in their composition due to attachments and shared components. Experimental and computational evidence indicate that consecutive addition and secondary losses of components played a major role in the evolution of some complexes, mostly without affecting the core function. Here, we analysed in a large scale approach whether this flexibility in evolution is only limited to a distinct number of complexes or represents a more general trend.ResultsFocussing on human protein complexes, we based our analysis on a manually curated dataset from HPRD. In total, 1,060 complexes with 6,136 proteins from 2,187 unique genes were considered. We computed interologs in 25 different species and predicted the composition of complexes. Over the analysed species, the composition of most complexes was highly flexible and only 25% of all genes were never lost. Even if one component was lost at a particular point in time, the fraction of observed second, independent losses of additional components was high (75% of all complexes affected). Still, loss of whole complexes happened rarely. This biological signal deviated significantly from random models. We exemplified this trend on the anaphase promoting complex (APC) where a core is highly conserved throughout all metazoans, but flexibility in certain components is observable.ConclusionConsecutive additions and losses of distinct units is a fundamental process in the evolution of protein complexes. These evolutionary events affecting genes coding for units in human protein complexes showed a significantly different phylogenetic pattern compared to randomly selected genes. Determination of taxon specific attachments or losses might be linked to specific cellular or morphological features. Thus, protein complexes contain not only structural and functional, but also evolutionary cores.

Dataset Information

Flexibility and constraint: Evolutionary remodeling of the sporulation initiation pathway in Firmicutes.

Publications

Flexibility and constraint: Evolutionary remodeling of the sporulation initiation pathway in Firmicutes.

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