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Santa Rosalia revisited: why are there so many species of bacteria?

The diversity of bacteria in the world is very poorly known. Usually less than one percent of the bacteria from natural communities can be grown in the laboratory. This has caused us to underestimate bacterial diversity and biased our view of bacterial communities. The tools are now available to estimate the number of bacterial species in a community and to estimate the difference between communities. Using what data are available, I have estimated that thirty grams of forest soil contains over half a million species. The species difference between related communities suggests that the number of species of bacteria may be more than a thousand million. I suppose that the explanation for such a large number of bacterial species is simply that speciation in bacteria is easy and extinction difficult, giving a rate of speciation higher than the rate of extinction, leading to an ever increasing number of species over time. The idea that speciation is easy is justified from the results of recent experimental work in bacterial evolution.

Bacteria↗

Genome evolution in enteric bacteria.

For more than a decade, the study of bacterial evolution has been dominated by the comparative analysis of nucleotide sequences within and among species. This approach, combined with the characterization of extensive regions of the chromosome by pulsed-field gel electrophoresis, has led to new insights into the dynamics of bacterial genomes.

Biological Evolution↗

Identification of interdomain sequences promoting the intronless evolution of a bacterial protein family.

In the evolution of eukaryotic genes, introns are believed to have played a major role in increasing the probability of favorable duplication events, chance recombinations, and exon shuffling resulting in functional hybrid proteins. As a rule, prokaryotic genes lack introns, and the examples of prokaryotic introns described do not seem to have contributed to gene evolution by exon shuffling. Still, certain protein families in modern bacteria evolve rapidly by recombination of genes, duplication of functional domains, and as shown for protein PAB of the anaerobic bacterial species Peptostreptococcus magnus, by the shuffling of an albumin-binding protein module from group C and G streptococci. Characterization of a protein PAB-related gene in a P. magnus strain with less albumin-binding activity revealed that the shuffled module was missing. Based on this fact and observations made when comparing gene sequences of this family of bacterial surface proteins interacting with albumin and/or immunoglobulin, a model is presented that can explain how this rapid intronless evolution takes place. A new kind of genetic element is introduced: the recer sequence promoting interdomain, in frame recombination and acting as a structure-less flexibility-promoting spacer in the corresponding protein. The data presented also suggest that antibiotics could represent the selective pressure behind the shuffling of protein modules in P. magnus, a member of the indigenous bacterial flora.

Albumins↗

Pathogenicity islands in bacterial pathogenesis.

In this review, we focus on a group of mobile genetic elements designated pathogenicity islands (PAI). These elements play a pivotal role in the virulence of bacterial pathogens of humans and are also essential for virulence in pathogens of animals and plants. Characteristic molecular features of PAI of important human pathogens and their role in pathogenesis are described. The availability of a large number of genome sequences of pathogenic bacteria and their benign relatives currently offers a unique opportunity for the identification of novel pathogen-specific genomic islands. However, this knowledge has to be complemented by improved model systems for the analysis of virulence functions of bacterial pathogens. PAI apparently have been acquired during the speciation of pathogens from their nonpathogenic or environmental ancestors. The acquisition of PAI not only is an ancient evolutionary event that led to the appearance of bacterial pathogens on a timescale of millions of years but also may represent a mechanism that contributes to the appearance of new pathogens within a human life span. The acquisition of knowledge about PAI, their structure, their mobility, and the pathogenicity factors they encode not only is helpful in gaining a better understanding of bacterial evolution and interactions of pathogens with eukaryotic host cells but also may have important practical implications such as providing delivery systems for vaccination, tools for cell biology, and tools for the development of new strategies for therapy of bacterial infections.

Bacteria↗

Retrotransfer of IncP plasmid R751 from Escherichia coli maxicells: evidence for the genetic sufficiency of self-transferable plasmids for bacterial conjugation.

Gene transfer between organisms is a prime contributor to evolution. Bacterial conjugation is probably the most important mechanism by which genes are spread among prokaryotes and perhaps also contributes to eukaryotic evolution. Conjugation is mediated by plasmids. The mechanism of conjugation remains ill-understood despite progress in the identification, mapping and sequencing of genes required for plasmid transmission. All conjugation-specific genes (those required only for DNA transfer and establishment) identified to date map to plasmids. We found that IncP plasmids could enter and subsequently convert maxicells, which are trapped in a metabolic state that prevents de novo expression of chromosomal genes, into conjugative donors. This suggests that IncP plasmids encode not only necessary functions but indeed all functions specific to DNA transmission. Thus, like viruses, plasmids can convert non-viable cells into gene vectors.

Chromosomes, Bacterial↗

Evolution of Staphylococcus aureus by large chromosomal replacements.

Conjugative transfer and replacement of hundreds of kilobases of a bacterial chromosome can occur in vitro, but replacements in nature are either an order of magnitude smaller or involve the movement of mobile genetic elements. We discovered that two lineages of Staphylococcus aureus, including a pandemic methicillin-resistant lineage, were founded by single chromosomal replacements of at least approximately 244 and approximately 557 kb representing approximately 10 and approximately 20% of the chromosome, respectively, without the obvious involvement of mobile genetic elements. The replacements are unprecedented in natural populations of bacteria because of their large size and unique structure and may have a dramatic impact on bacterial evolution.

Base Sequence↗

Host-driven evolution shapes the polysaccharide utilization profiles of alga-associated Flavobacteriaceae.

BACKGROUND: Marine algae represent major producers of complex polysaccharides and serve as hosts for diverse microbial communities in the phycosphere. Flavobacteriaceae are among the key bacterial taxa involved in polysaccharide degradation and carbon remineralization in this environment. However, the extent to which algal hosts drive the divergence of polysaccharide utilization profiles in these bacteria remains unclear. RESULTS: We conducted a genome-resolved analysis of 103 cultured Flavobacteriaceae strains isolated from red, green, and brown macroalgae, as well as from diatoms and dinoflagellates. We found that macroalga-associated strains generally harbored more abundant and diverse CAZyme-encoding genes than their microalga-associated counterparts. Moreover, strains associated with different algal phyla showed distinct metabolic specializations that aligned with the typical polysaccharides of their respective hosts, strongly supporting host-specific adaptation. In four widely distributed genera (Maribacter, Flagellimonas, Polaribacter, Winogradskyella), CAZyme profile dissimilarity and key glycoside hydrolase gene divergence exhibited phylogenetic congruence with algal host phylogeny (Mantel r up to 0.76 and 0.85, respectively), indicative of host-associated functional adaptation. Using Maribacter as a model, cultivation experiments and transcriptome characterization demonstrated that polysaccharide utilization efficiency is not solely linked to the organization of genes into polysaccharide utilization loci (PULs), but also associated with the expression dynamics of key transcription factors (TFs), particularly those from AraC and DeoR families, whose expression patterns were coordinated with laminarin degradation. Notably, these two TF families also exhibited host-associated divergence patterns similar to those of CAZyme-encoding genes. Furthermore, analysis of the Tara Oceans metagenomic data indicated that, within the AraC and DeoR families, a higher proportion of genes were positively correlated with chlorophyll a content compared to other TF families, reinforcing their specialized roles in alga-associated bacterial lifestyles. CONCLUSIONS: Our integrative genomic and transcriptomic analyses reveal evolutionary and regulatory adaptation of marine Flavobacteriaceae to distinct algal hosts. These findings highlight algae-derived habitats as specialized niches that shape microbial metabolic potential, and suggest that carbohydrate metabolism plays a key role in host-driven bacterial evolution across global oceans. Video Abstract.

Flavobacteriaceae↗

On the origin of Ser/Thr kinases in a prokaryote.

The family of Ser/Thr and/or Tyr kinases and that of His kinases play essential roles in signal transduction. For a long time, the former has been found in eukaryotes, the latter in prokaryotes. Studies in the last decade have shown, however, that most bacteria possess from one to more than 10 genes encoding Ser/Thr kinases. This observation raises an important question concerning the evolutionary origin of Ser/Thr kinases found in bacteria. To answer this question, we have analyzed a family of 11 genes encoding Ser/Thr kinases in the cyanobacterium Synechocystis sp. PCC 6803. This bacterium contains the largest number of Ser/Thr kinases among all bacteria whose genomic sequences have been released so far. In this study, we have developed a user-friendly computer program for statistical analysis of codon usages and GC content. The results demonstrate that Ser/Thr kinases have similar codon usages and GC contents as the average of all possible open reading frames (ORFs) deduced from the genome. In contrast, ORFs encoding transposases, as a control in our analysis, display a disparity in both codon usage and GC content, confirming their multiple origin and genetic promiscuity. In light of our results, we propose that Ser/Thr kinases existed before the divergence between prokaryotes and eukaryotes during evolution, or were laterally transferred into prokaryotes at the early stages of bacterial evolution. If Ser/Thr kinases have persisted ever since in prokaryotes under evolutionary pressure, it is then expected that they play important, possibly even essential roles in regulating bacterial activities as do their counterparts in eukaryotes.

Base Composition↗

Evolution in bacteria: evidence for a universal substitution rate in cellular genomes.

This paper constructs a temporal scale for bacterial evolution by tying ecological events that took place at known times in the geological past to specific branch points in the genealogical tree relating the 16S ribosomal RNAs of eubacteria, mitochondria, and chloroplasts. One thus obtains a relationship between time and bacterial RNA divergence which can be used to estimate times of divergence between other branches in the bacterial tree. According to this approach, Salmonella typhimurium and Escherichia coli diverged between 120 and 160 million years (Myr) ago, a date which fits with evidence that the chief habitats occupied now by these two enteric species became available that long ago. The median extent of divergence between S. typhimurium and E. coli at synonymous sites for 21 kilobases of protein-coding DNA is 100%. This implies a silent substitution rate of 0.7-0.8%/Myr--a rate remarkably similar to that observed in the nuclear genes of mammals, invertebrates, and flowering plants. Similarities in the substitution rates of eucaryotes and procaryotes are not limited to silent substitutions in protein-coding regions. The average substitution rate for 16S rRNA in eubacteria is about 1%/50 Myr, similar to the average rate for 18S rRNA in vertebrates and flowering plants. Likewise, we estimate a mean rate of roughly 1%/25 Myr for 5S rRNA in both eubacteria and eucaryotes. For a few protein-coding genes of these enteric bacteria, the extent of silent substitution since the divergence of S. typhimurium and E. coli is much lower than 100%, owing to extreme bias in the usage of synonymous codons. Furthermore, in these bacteria, rates of amino acid replacement were about 20 times lower, on average, than the silent rate. By contrast, for the mammalian genes studied to date, the average replacement rate is only four to five times lower than the rate of silent substitution.

Bacteria↗

Hypervariable DNA fingerprinting in Escherichia coli: minisatellite probe from bacteriophage M13.

Extensive restriction-fragment-length polymorphism was revealed in Escherichia coli strains by using a region of the bacteriophage M13 genome as a DNA hybridization probe. This variation was observed across natural strains, in clinical samples, and to a lesser extent in laboratory strains. The sequence in M13 which revealed this fingerprint pattern was a region of the gene III coat protein, which contains two clusters of a 15-base-pair repeat. Oligonucleotides made to a consensus of these repeats also revealed the fingerprint profile. While this consensus sequence has significant homology to the lambda chi site sequence, an oligonucleotide made of the chi sequence did not reveal polymorphic fingerprint patterns in E. coli. The strain variation revealed by the M13 and M13-derived oligonucleotide probes will be useful for bacterial characterization and should find use in studies of bacterial evolution and population dynamics. The findings raise questions about what these repeated sequences are and why they are so variable.

Biological Evolution↗

Evolutionary significance of stress-induced mutagenesis in bacteria.

Mutagenesis is often increased in bacterial populations as a consequence of stress-induced genetic pathways. Analysis of the molecular mechanisms involved suggests that mutagenesis might be increased as a by-product of the stress response of the organism. By contrast, computer simulations and analyses of stress-inducible phenotypes among natural isolates of Escherichia coli suggest that stress-induced mutagenesis (SIM) could be the result of selection because of the beneficial mutations that such a process can potentially generate. Regardless of the nature of the selective pressure acting on SIM, it is possible that the resulting increased genetic variability plays an important role in bacterial evolution.

Adaptation, Biological↗

Genome organization, natural genetic engineering and adaptive mutation.

Bacterial evolution is considered in the light of molecular discoveries about genome organization, biochemical mechanisms of genetic change, and cellular control networks. Prokaryotic genetic determinants are organized as modular composites of coding sequences and protein-factor binding sites joined together during evolution. Studies of genetic change have revealed the existence of biochemical functions capable of restructuring the bacterial genome at various levels and joining together different sequence elements. These natural genetic engineering systems can be subject to regulation by signal transduction networks conveying information about the extracellular and intracellular environments. Mu-mediated araB-lacZ coding sequence fusions provide one example of adaptive mutation (increased formation of useful mutations under selection) and illustrate how physiological regulation can modulate the activity of a natural genetic engineering system under specific conditions.

Bacteria↗

H-NS, the genome sentinel.

Two recent reports have indicated that the H-NS protein in Salmonella enterica serovar Typhimurium has a key role in selectively silencing the transcription of large numbers of horizontally acquired AT-rich genes, including those that make up its major pathogenicity islands. Broadly similar conclusions have emerged from a study of H-NS binding to DNA in Escherichia coli. How do these findings affect our view of H-NS and its ability to influence bacterial evolution?

AT Rich Sequence↗

Distribution and sequence analysis of a family of type ill-dependent effectors correlate with the phylogeny of Ralstonia solanacearum strains.

In Ralstonia solanacearum, we previously have reported on the characterization of popP1 and popP2 genes. These genes encode type III-dependent pathogenicity effectors related to the large family of AvrRxv/YopJ cysteine proteases that are shared among pathogens of plants and animals. In this study, we identify a third gene, named popP3, that is inactivated in the genome sequence of strain GMI1000 by insertion of a copy of the insertion sequence ISRso13. The three popP genes are localized on two large chromosomal pathogenicity islands, with popP1 and popP2 being present on the same island. Phylogenic analysis demonstrated that the PopP2 and PopP3 proteins are clearly distinct from other effectors of this family previously characterized in plant and animal pathogens. Analysis of the distribution and allelic variations of the three genes in 30 strains representative of the biodiversity of R. solanacearum established that popP genes are distributed widely among strains from two of the three phyla previously defined on the basis of the structure of the core genome. Sequencing of the popP genes from the different strains revealed limited allelic variations at the three loci but did not show evidence of recombination between the popP genes. Limited allelic variation together with occurrence of insertion sequences within or in the close vicinity of popP genes and the presence of gene duplications in these pathogenicity islands suggest that genomic rearrangements might be a major evolutionary driving force controlling evolution of the genes encoded in these regions. The implications of these observations in terms of bacterial evolution, gene acquisition, and horizontal gene transfers are discussed.

Alleles↗

Phylogeny of gamma-proteobacteria: resolution of one branch of the universal tree?

The reconstruction of bacterial evolutionary relationships has proven to be a daunting task because variable mutation rates and horizontal gene transfer (HGT) among species can cause grave incongruities between phylogenetic trees based on single genes. Recently, a highly robust phylogenetic tree was constructed for 13 gamma-proteobacteria using the combined alignments of 205 conserved orthologous proteins.1 Only two proteins had incongruent tree topologies, which were attributed to HGT between Pseudomonas species and Vibrio cholerae or enterics. While the evolutionary relationships among these species appears to be resolved, further analysis suggests that HGT events with other bacterial partners likely occurred; this alters the implicit assumption of gamma-proteobacteria monophyly. Thus, any thorough reconstruction of bacterial evolution must not only choose a suitable set of molecular markers but also strive to reduce potential bias in the selection of species.

Bacterial Proteins↗

A model combining cell physiology and population genetics to explain Escherichia coli laboratory evolution.

BACKGROUND: Laboratory experiments under controlled conditions during thousands of generations are useful tools to assess the processes underlying bacterial evolution. As a result of these experiments, the way in which the traits change in time is obtained. Under these conditions, the bacteria E. coli shows a parallel increase in cell volume and fitness. RESULTS: To explain this pattern it is required to consider organismic and population contributions. For this purpose we incorporate relevant information concerning bacterial structure, composition and transformations in a minimal modular model. In the short time scale, the model reproduces the physiological responses of the traits to changes in nutrient concentration. The decay of unused catabolic functions, found experimentally, is introduced in the model using simple population genetics. The resulting curves representing the evolution of volume and fitness in time are in good agreement with those obtained experimentally. CONCLUSIONS: This study draws attention on physiology when studying evolution. Moreover, minimal modular models appear to be an adequate strategy to unite these barely related disciplines of biology.

Cell Cycle↗

Dichotomy of major bacterial phyla inferred from gene arrangement comparisons.

A computer search for gene arrangements that are present in Gram-positive bacteria but are absent from Proteobacteria and vice versa was carried out. Four such arrangements were detected, based on which major bacterial phyla were divided into two groups; Thermotoga, Deinococcus-Thermus, Chloroflexi (green non-sulfur bacteria), and Fusobacteria, represent Gram-positive bacterial gene arrangements, while Aquifex, Spirochetes, Planctomycetes, Chlorobi (green sulfur bacteria), Bacteroides show Proteobacterial arrangements. The division is almost consistent with another partition of the major phyla based on the comparison of domain architectures of RNA polymerase subunits and sigma factor, suggesting a fundamental split of the major bacterial phyla at an early stage of bacterial evolution.

Bacteria↗