Prokaryotic Pangenomes Act as Evolving Ecosystems

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Abstract

Understanding adaptation to the local environment is a central tenet and a major focus of evolutionary biology. But this is only part of the adaptionist story. In addition to the external environment, one of the main drivers of genome composition is genetic background. In this perspective, I argue that there is a growing body of evidence that intra-genomic selective pressures play a significant part in the composition of prokaryotic genomes and play a significant role in the origin, maintenance and structuring of prokaryotic pangenomes.

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Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial "pan-genome".

H Tettelin, V Masignani, M. J. Cieslewicz … (2005)

The development of efficient and inexpensive genome sequencing methods has revolutionized the study of human bacterial pathogens and improved vaccine design. Unfortunately, the sequence of a single genome does not reflect how genetic variability drives pathogenesis within a bacterial species and also limits genome-wide screens for vaccine candidates or for antimicrobial targets. We have generated the genomic sequence of six strains representing the five major disease-causing serotypes of Streptococcus agalactiae, the main cause of neonatal infection in humans. Analysis of these genomes and those available in databases showed that the S. agalactiae species can be described by a pan-genome consisting of a core genome shared by all isolates, accounting for approximately 80% of any single genome, plus a dispensable genome consisting of partially shared and strain-specific genes. Mathematical extrapolation of the data suggests that the gene reservoir available for inclusion in the S. agalactiae pan-genome is vast and that unique genes will continue to be identified even after sequencing hundreds of genomes.

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The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss

J Morris, Richard Lenski, Erik R. Zinser (2012)

ABSTRACT Reductive genomic evolution, driven by genetic drift, is common in endosymbiotic bacteria. Genome reduction is less common in free-living organisms, but it has occurred in the numerically dominant open-ocean bacterioplankton Prochlorococcus and “Candidatus Pelagibacter,” and in these cases the reduction appears to be driven by natural selection rather than drift. Gene loss in free-living organisms may leave them dependent on cooccurring microbes for lost metabolic functions. We present the Black Queen Hypothesis (BQH), a novel theory of reductive evolution that explains how selection leads to such dependencies; its name refers to the queen of spades in the game Hearts, where the usual strategy is to avoid taking this card. Gene loss can provide a selective advantage by conserving an organism’s limiting resources, provided the gene’s function is dispensable. Many vital genetic functions are leaky, thereby unavoidably producing public goods that are available to the entire community. Such leaky functions are thus dispensable for individuals, provided they are not lost entirely from the community. The BQH predicts that the loss of a costly, leaky function is selectively favored at the individual level and will proceed until the production of public goods is just sufficient to support the equilibrium community; at that point, the benefit of any further loss would be offset by the cost. Evolution in accordance with the BQH thus generates “beneficiaries” of reduced genomic content that are dependent on leaky “helpers,” and it may explain the observed nonuniversality of prototrophy, stress resistance, and other cellular functions in the microbial world.

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Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli.

R Welch, V Burland, G Plunkett … (2002)

We present the complete genome sequence of uropathogenic Escherichia coli, strain CFT073. A three-way genome comparison of the CFT073, enterohemorrhagic E. coli EDL933, and laboratory strain MG1655 reveals that, amazingly, only 39.2% of their combined (nonredundant) set of proteins actually are common to all three strains. The pathogen genomes are as different from each other as each pathogen is from the benign strain. The difference in disease potential between O157:H7 and CFT073 is reflected in the absence of genes for type III secretion system or phage- and plasmid-encoded toxins found in some classes of diarrheagenic E. coli. The CFT073 genome is particularly rich in genes that encode potential fimbrial adhesins, autotransporters, iron-sequestration systems, and phase-switch recombinases. Striking differences exist between the large pathogenicity islands of CFT073 and two other well-studied uropathogenic E. coli strains, J96 and 536. Comparisons indicate that extraintestinal pathogenic E. coli arose independently from multiple clonal lineages. The different E. coli pathotypes have maintained a remarkable synteny of common, vertically evolved genes, whereas many islands interrupting this common backbone have been acquired by different horizontal transfer events in each strain.

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Author and article information

Contributors

James O McInerney:

ORCID: https://orcid.org/0000-0003-1885-2503

Dr Brandon Gaut: Role: Associate Editor

Journal

Journal ID (nlm-ta): Mol Biol Evol

Journal ID (iso-abbrev): Mol Biol Evol

Journal ID (publisher-id): molbev

Title: Molecular Biology and Evolution

Publisher: Oxford University Press (US )

ISSN (Print): 0737-4038

ISSN (Electronic): 1537-1719

Publication date Collection: January 2023

Publication date (Electronic): 27 October 2022

Publication date PMC-release: 27 October 2022

Volume: 40

Issue: 1

Electronic Location Identifier: msac232

Affiliations

School of Life Sciences, The University of Nottingham, University Park , Nottingham NG7 2UH, UK

Author notes

Corresponding author: E-mail: james.mcinerney@ 123456nottingham.ac.uk

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James O McInerney https://orcid.org/0000-0003-1885-2503

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Publisher ID: msac232

DOI: 10.1093/molbev/msac232

PMC ID: 9851318

PubMed ID: 36288801

SO-VID: 9f1e79fe-b1c3-4e79-ad5a-d5a9cb13f7e9

License:

This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

Prokaryotic Pangenomes Act as Evolving Ecosystems

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Abstract

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IUCN Red List of Ecosystems

Most cited references 48

Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial "pan-genome".

The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss

Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli.

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