Evolution and the complexity of bacteriophages - PubMed (original) (raw)

Evolution and the complexity of bacteriophages

Philip Serwer. Virol J. 2007.

Abstract

Background: The genomes of both long-genome (> 200 Kb) bacteriophages and long-genome eukaryotic viruses have cellular gene homologs whose selective advantage is not explained. These homologs add genomic and possibly biochemical complexity. Understanding their significance requires a definition of complexity that is more biochemically oriented than past empirically based definitions.

Hypothesis: Initially, I propose two biochemistry-oriented definitions of complexity: either decreased randomness or increased encoded information that does not serve immediate needs. Then, I make the assumption that these two definitions are equivalent. This assumption and recent data lead to the following four-part hypothesis that explains the presence of cellular gene homologs in long bacteriophage genomes and also provides a pathway for complexity increases in prokaryotic cells: (1) Prokaryotes underwent evolutionary increases in biochemical complexity after the eukaryote/prokaryote splits. (2) Some of the complexity increases occurred via multi-step, weak selection that was both protected from strong selection and accelerated by embedding evolving cellular genes in the genomes of bacteriophages and, presumably, also archaeal viruses (first tier selection). (3) The mechanisms for retaining cellular genes in viral genomes evolved under additional, longer-term selection that was stronger (second tier selection). (4) The second tier selection was based on increased access by prokaryotic cells to improved biochemical systems. This access was achieved when DNA transfer moved to prokaryotic cells both the more evolved genes and their more competitive and complex biochemical systems.

Testing the hypothesis: I propose testing this hypothesis by controlled evolution in microbial communities to (1) determine the effects of deleting individual cellular gene homologs on the growth and evolution of long genome bacteriophages and hosts, (2) find the environmental conditions that select for the presence of cellular gene homologs, (3) determine which, if any, bacteriophage genes were selected for maintaining the homologs and (4) determine the dynamics of homolog evolution.

Implications of the hypothesis: This hypothesis is an explanation of evolutionary leaps in general. If accurate, it will assist both understanding and influencing the evolution of microbes and their communities. Analysis of evolutionary complexity increase for at least prokaryotes should include analysis of genomes of long-genome bacteriophages.

PubMed Disclaimer

Figures

Figure 1

Figure 1

Initiation of DNA packaging by the closely related bacteriophages, T3 and T7. (a) Initiation is illustrated for the simplest DNA packaging. This packaging has a monomeric DNA substrate and was demonstrated for T3 and assumed for T7. Packaging of this type occurs only in vitro, as far as is known (review [31,32]). (b) Initiation is illustrated for the more complex DNA packaging that occurs in vivo for both T3 and T7 (review [31,32]). In (b), the DNA substrate is an end-to-end joined concatemeric DNA for which only one monomer is completely shown. Dashed lines in (b) indicate part of another monomer within the concatemer. The following details of the concatemer are omitted for simplicity: replication forks and interaction among different procapsids (review [32]). The various proteins and protein assemblies of the initiation complex, including the connector and DNA packaging ATPase, are identified in the rectangular box. Proteins have both descriptive names and names based on gene number [2], preceded by gp. The letter, R, indicates the right end of the mature DNA molecule; the letter, L, indicates the left end.

Similar articles

Cited by

References

    1. Jardine PJ, Anderson DL. DNA packaging in dsDNA bacteriophages. In: Calendar R, editor. The Bacteriophages. New York: Oxford University Press; 2006.
    1. Pajunen MI, Elizondo MR, Skurnik M, Kieleczawa J, Molineux IJ. Complete nucleotide sequence and likely recombinatorial origin of bacteriophage T3. J Mol Biol. 2003;319:1115–1132. doi: 10.1016/S0022-2836(02)00384-4. - DOI - PubMed
    1. Meijer WJ, Horcajadas JA, Salas M. φ 29 family of phages. Microbiol Mol Biol Rev. 2001;65:261–287. doi: 10.1128/MMBR.65.2.261-287.2001. - DOI - PMC - PubMed
    1. Kutter E, Stidham T, Guttman B, Kutter E, Batts D, Peterson S, Djavakhishvili T, Arisaka F, Mesyanzhinov V, Rüger W, Mosig G. Genomic map of bacteriophage T4. In: Karam JD, editor. Molecular Biology of Bacteriophage T4. Washington, DC: ASM Press; 1994. pp. 491–519.
    1. Miller ES, Heidelberg JF, Eisen JA, Nelson WC, Durkin AS, Ciecko A, Feldblyum TV, White O, Paulsen IT, Nierman WC, Lee J, Szczypinski B, Fraser CM. Complete genome sequence of the broad-host-range vibriophage KVP40: comparative genomics of a T4-related bacteriophage. J Bacteriol. 2003;185:5220–5233. doi: 10.1128/JB.185.17.5220-5233.2003. - DOI - PMC - PubMed

Publication types

MeSH terms

Substances

LinkOut - more resources