Evolution of microbes and viruses: a paradigm shift in evolutionary biology?

Abstract

When Charles Darwin formulated the central principles of evolutionary biology in the Origin of Species in 1859 and the architects of the Modern Synthesis integrated these principles with population genetics almost a century later, the principal if not the sole objects of evolutionary biology were multicellular eukaryotes, primarily animals and plants. Before the advent of efficient gene sequencing, all attempts to extend evolutionary studies to bacteria have been futile. Sequencing of the rRNA genes in thousands of microbes allowed the construction of the three- domain "ribosomal Tree of Life" that was widely thought to have resolved the evolutionary relationships between the cellular life forms. However, subsequent massive sequencing of numerous, complete microbial genomes revealed novel evolutionary phenomena, the most fundamental of these being: (1) pervasive horizontal gene transfer (HGT), in large part mediated by viruses and plasmids, that shapes the genomes of archaea and bacteria and call for a radical revision (if not abandonment) of the Tree of Life concept, (2) Lamarckian-type inheritance that appears to be critical for antivirus defense and other forms of adaptation in prokaryotes, and (3) evolution of evolvability, i.e., dedicated mechanisms for evolution such as vehicles for HGT and stress-induced mutagenesis systems. In the non-cellular part of the microbial world, phylogenomics and metagenomics of viruses and related selfish genetic elements revealed enormous genetic and molecular diversity and extremely high abundance of viruses that come across as the dominant biological entities on earth. Furthermore, the perennial arms race between viruses and their hosts is one of the defining factors of evolution. Thus, microbial phylogenomics adds new dimensions to the fundamental picture of evolution even as the principle of descent with modification discovered by Darwin and the laws of population genetics remain at the core of evolutionary biology.

Keywords: Darwin; comparative genomics; horizontal gene transfer; modern synthesis; tree of life.

Figure 1

The three-domain tree of life: a generalized schematic, A, Archaea, B, bacteria, E, Eukaryota.

Figure 2

A network representation of the evolutionary process. The network still includes some tree components such that the three domains of cellular life remains distinct but there is also an extensive horizontal component of genetic information flow that in particular dominates the earliest stages of evolution (Koonin and Wolf, 2008).

Figure 3

Tree-like (vertical) and web-like (horizontal) contributions in the evolution of nearly universal genes and the entire phylogenetic forest. The two heat maps schematically depict comparison of bacterial and archaeal genomes as described previously (Puigbo et al., 2010).

Figure 4

The universal distribution of gene commonality in the microbial genomic universe: a generalized schematic. The three broken lines represent three exponential functions that fit the core (on the right), the shell (in the middle) and the cloud (on the left) of prokaryotic genes (O'Malley and Koonin, 2011).

Figure 5

The core, shell, and cloud of microbial genes. A generalized schematic showing the approximate contributions of the core, shell, and cloud to the pangenomes of prokaryotes and individual genomes.

Figure 6

The continuum of evolutionary processes, from stochasticity to determinism.

Figure 7

The viral and cellular “empires” of life forms and domains within them. The cellular empire domains: A, Archaea; B, Bacteria; E, Eukaryota. The Virus empire domains: +R, positive-strand RNA viruses; −R, negative-strand RNA viruses; dsR, double-stranded RNA viruses; dsD, double-stranded DNA viruses; ssD, single-stranded DNA viruses; RT, retro-transcribing elements/viruses; VR, viroids.

Figure 8

The conceptual structure of evolutionary biology: the Darwinian core and the new levels of complexity.