Conserved Gene Clusters in Bacterial Genomes Provide Further Support for the Primacy of RNA

Siefert, Janet L.; Martin, Kirt; Abdi, Fadi; Widger, William R.; Fox, George E.

doi:10.1007/pl00006251

Cited by 56 publications

(39 citation statements)

References 20 publications

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“…Hence there is a possible conflict between the organismal and cellular levels of selection: the multicellular organism would benefit from a redundant (flatter) fitness landscape, whereas the cells of which the organism is composed would benefit from an antiredundant (steeper) landscape. Interestingly, in some cases this conflict has a synergistic resolution: antiredundancy at the cellular level is an effective means of ensuring redundancy and robustness at the Gene duplication (14) Overlapping reading frames (9) Neutral codon usage (25) Nonconservative codon bias (26) -Gene silencing (27) Polyploidy (28) Haploidy Multiple regulatory elements for n genes (29) Single regulatory element for n genes Chaperone and heat shock proteins (30,31) Checkpoint genes promoting repair (32) Checkpoint genes inducing apoptosis (33) Telomerase induction (34) Loss of telomerase (35) Dominance (36,37) Incomplete dominance Autophagy (38,39) mRNA surveillance (40,41) Bulk transmission (42,43) Bottlenecks in transmission (44, 45) Molecular quality control (46) tRNA suppressor molecules (47) Modularity (48) Multiple organelle copies (49) Single organelle copies Parallel metabolic pathways (6,50) Serial metabolic pathways Correlated gene expression (29,51) Uncorrelated gene expression DNA error repair (52) Loss of error repair (53)(54)(55) Redundant mechanisms mask the phenotypic effect of mutations, allowing the mutations to persist in populations. We group together these mechanisms with a small s value.…”

Section: Redundancy and Levels Of Selectionmentioning

confidence: 99%

Redundancy, antiredundancy, and the robustness of genomes

Krakauer

Plotkin

2002

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

228

225

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Genetic mutations that lead to undetectable or minimal changes in phenotypes are said to reveal redundant functions. Redundancy is common among phenotypes of higher organisms that experience low mutation rates and small population sizes. Redundancy is less common among organisms with high mutation rates and large populations, or among the rapidly dividing cells of multicellular organisms. In these cases, one even observes the opposite tendency: a hypersensitivity to mutation, which we refer to as antiredundancy. In this paper we analyze the evolutionary dynamics of redundancy and antiredundancy. Assuming a cost of redundancy, we find that large populations will evolve antiredundant mechanisms for removing mutants and thereby bolster the robustness of wild-type genomes; whereas small populations will evolve redundancy to ensure that all individuals have a high chance of survival. We propose that antiredundancy is as important for developmental robustness as redundancy, and is an essential mechanism for ensuring tissue-level stability in complex multicellular organisms. We suggest that antiredundancy deserves greater attention in relation to cancer, mitochondrial disease, and virus infection.genomic stability ͉ mutation selection ͉ canalization ͉ fitness landscape ͉ quasispecies

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Section: Redundancy and Levels Of Selectionmentioning

confidence: 99%

Redundancy, antiredundancy, and the robustness of genomes

Krakauer

Plotkin

2002

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

228

225

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“…Early comparisons of sequenced genomes detected little long-range conservation in gene order (Mushegan and Koonin 1996); but overlaid on this pattern, there are several gene clusters and gene pairs (mostly involving ribosomal proteins) maintained in all bacterial genomes (Siefert et al 1997, Dandekar et al 1998, Wachterhauser 1998, Wolf et al 2001). Conservation of gene order seems to reflect the evolutionary distance between organisms (Tamames 2000, Wolf et al 2001), but it evolves faster than gene contents Bork 1998, Korbel et al 2002), and its use as a phylogentic marker should be limited to comparisons of rather closely related genomes (Suyama and Bork 2001).…”

Section: Looking Beyond Sequence Evolutionmentioning

confidence: 99%

Phylogenetic Relationships of Bacteria with Special Reference to Endosymbionts and Enteric Species

Francino¹,

Santos²,

Ochman³

2006

The Prokaryotes

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INTRODUCTIONThe latter half of the 20 th century saw two developments that revolutionized the study of bacterial systematics and our conceptions about microbial diversity. The first was the use of molecular genetic information, as gained through the analysis of protein and nucleic acid sequences, for the identification, typing and classification of microorganisms. The second was the application of PCR for the recovery of DNA sequences from non-cultivable organisms.By decoupling cultivation and classification, and by providing a common yardstick by which all organisms could be compared (i.e., small subunit ribosomal DNA sequences; hereafter referred to as SSU rRNA), these procedures added a new dimension to our knowledge of the microbial world. It is no longer necessary to test organisms against a panel of known phenotypic or biochemical properties, which, in themselves, are often variable in occurrence and can lead to cases of misclassification, or carry a preconceived notion about the characters that define a particular taxonomic group.Despite the considerable advances made from applying these innovations, such an approach is not without its limitations. Characterization of a single conserved sequence, while often adequate for taxonomic purposes, does not reveal very much about the evolutionary history or biology of the organism per se. Whereas the placement of an organism (i.e., sequence) into an evolutionary framework may prompt numerous predictions about its morphology, ecology, physiology and biochemistry, virtually nothing can be said about its unique biology without cultivation or additional sequence information.Other problems can arise when attempting to classify bacteria and to determine their relationships. These derive from two sources: the specific characters used to represent an organism (the choice of data), and the algorithms used to infer relationships (the methods used to construct the phylogeny or tree). With this in mind, genotypic data hold several advantages over phenotypic characters for phylogenetic reconstruction in that: (i) variation in molecular sequences is discrete and well-defined; (ii) molecular sequences comprise hundreds, if not thousands, of characters bearing potentially useful information; (iii) molecular sequences accumulate informative changes, even when the resulting phenotypes are conserved; (iv) informational macromolecules (DNA and proteins) change according to well-defined models of sequence evolution; and (v) identical phenotypes can arise by very different genetic mechanisms or pathways, such that changes other than those attributable to common ancestry can lead to the same phenotype.Questions of character convergence are not limited to phenotypic traits: portions of molecular sequences may be identical due to chance, natural selection, or lateral gene transfer.Furthermore, because the analysis of relatively small regions of DNA can furnish so much information, phylogenetic relationships are often based on data collected from a very limited portion of the genome, w...

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“…Several comparative studies of bacterial, archaeal, and eukaryotic genomes have concluded that, in general, gene order is not conserved (Himmelreich et al 1997;Kolstø 1997;Koonin and Galperin 1997;Siefert et al 1997;Watanabe et al 1997;Dandekar et al 1998;Rocha 2008). In stark contrast, gene order within virus orders and families is often conserved.…”

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confidence: 99%

Multiple Barriers to the Evolution of Alternative Gene Orders in a Positive-Strand RNA Virus

et al. 2016

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The order in which genes are organized within a genome is generally not conserved between distantly related species. However, within virus orders and families, strong conservation of gene order is observed. The factors that constrain or promote gene-order diversity are largely unknown, although the regulation of gene expression is one important constraint for viruses. Here we investigate why gene order is conserved for a positive-strand RNA virus encoding a single polyprotein in the context of its authentic multicellular host. Initially, we identified the most plausible trajectory by which alternative gene orders could evolve. Subsequently, we studied the accessibility of key steps along this evolutionary trajectory by constructing two virus intermediates: (1) duplication of a gene followed by (2) loss of the ancestral gene. We identified five barriers to the evolution of alternative gene orders. First, the number of viable positions for reordering is limited. Second, the within-host fitness of viruses with gene duplications is low compared to the wild-type virus. Third, after duplication, the ancestral gene copy is always maintained and never the duplicated one. Fourth, viruses with an alternative gene order have even lower fitness than viruses with gene duplications. Fifth, after more than half a year of evolution in isolation, viruses with an alternative gene order are still vastly inferior to the wild-type virus. Our results show that all steps along plausible evolutionary trajectories to alternative gene orders are highly unlikely. Hence, the inaccessibility of these trajectories probably contributes to the conservation of gene order in present-day viruses.

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Conserved Gene Clusters in Bacterial Genomes Provide Further Support for the Primacy of RNA

Cited by 56 publications

References 20 publications

Redundancy, antiredundancy, and the robustness of genomes

Redundancy, antiredundancy, and the robustness of genomes

Phylogenetic Relationships of Bacteria with Special Reference to Endosymbionts and Enteric Species

Multiple Barriers to the Evolution of Alternative Gene Orders in a Positive-Strand RNA Virus

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