A null model for microbial diversification

Abstract

Whether prokaryotes (Bacteria and Archaea) are naturally organized into phenotypically and genetically cohesive units comparable to animal or plant species remains contested, frustrating attempts to estimate how many such units there might be, or to identify the ecological roles they play. Analyses of gene sequences in various closely related prokaryotic groups reveal that sequence diversity is typically organized into distinct clusters, and processes such as periodic selection and extensive recombination are understood to be drivers of cluster formation ("speciation"). However, observed patterns are rarely compared with those obtainable with simple null models of diversification under stochastic lineage birth and death and random genetic drift. Via a combination of simulations and analyses of core and phylogenetic marker genes, we show that patterns of diversity for the genera ,, and are generally indistinguishable from patterns arising under a null model. We suggest that caution should thus be taken in interpreting observed clustering as a result of selective evolutionary forces. Unknown forces do, however, appear to play a role in, and some individual genes in all groups fail to conform to the null model. Taken together, we recommend the presented birth-death model as a null hypothesis in prokaryotic speciation studies. It is only when the real data are statistically different from the expectations under the null model that some speciation process should be invoked.

A census-based estimate of Earth's bacterial and archaeal diversity

“…Note that one important and potentially wrong assumption of this model is that cell turnover is statistically independent of phylogeny. A similar model was recently proposed by Straub and colleagues [78] as a null model for 16S phylogenies. Based on our model, we predict that there should exist about OTUs (assuming N = 10 30 [79] and [80,81], details in S2 Text).…”

High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries

“…The biological mechanisms underlying this genetic discontinuity are not clear but should be subject of future research for a more complete understanding of prokaryotic species. The mechanisms could involve a dramatic drop in recombination frequency around 90–95% ANI, which could account for the discontinuity if bacteria evolve sexually 33 , ecological sweeps that remove diversity due to competition 34 , 35 , or stochastic neutral processes 36 , 37 . A genomic nucleotide diversity of 5–10% translates to tens of thousands of years of evolution time, which provides ample opportunities for ecological or genetic sweeps to occur.…”

Sequence‐discrete species for prokaryotes and other microbes: A historical perspective and pending issues

“…The high consistency in terms of the 90%-95% ANI representing the area of discreteness between closely related species across different microbial taxa implies that a common mechanism(s) may underlie these diversity patterns. While random death and birth (speciation) could provide sequence-discrete clusters similar to those described above (Figure 1) 38 , obtaining clusters with the area of intercluster discreteness to be centered around the exact same ANI value (i.e., 90%-95%) across taxa with different lifestyles (e.g., symbiotic vs. free-living), habitats, or even informational material (e.g., DNA vs. RNA viruses) just based on random processes seems rather unlikely. Instead, a genetic (e.g., recombination, selection for specific mutations) and/or an ecological mechanism (e.g., functional differentiation in response to changing growth conditions) must be at play.…”