Polynucleobacter necessarius, a model for genome reduction in both free-living and symbiotic bacteria

Abstract

We present the complete genomic sequence of the essential symbiont Polynucleobacter necessarius (Betaproteobacteria), which is a valuable case study for several reasons. First, it is hosted by a ciliated protist, Euplotes; bacterial symbionts of ciliates are still poorly known because of a lack of extensive molecular data. Second, the single species P. necessarius contains both symbiotic and free-living strains, allowing for a comparison between closely related organisms with different ecologies. Third, free-living P. necessarius strains are exceptional by themselves because of their small genome size, reduced metabolic flexibility, and high worldwide abundance in freshwater systems. We provide a comparative analysis of P. necessarius metabolism and explore the peculiar features of a genome reduction that occurred on an already streamlined genome. We compare this unusual system with current hypotheses for genome erosion in symbionts and free-living bacteria, propose modifications to the presently accepted model, and discuss the potential consequences of translesion DNA polymerase loss.

Keywords: Burkholderiales; genome streamlining; nonsynonymous mutation rates; protozoa; symbiosis.

Fig. 1.

Percentage allocation of coding and noncoding DNA in the free-living and symbiotic Polynucleobacter genomes. The graph areas are proportional to genome sizes (2.16 and 1.56 Mbp, respectively). Pseudogenes were identified with a more conservative (*) and a more permissive (**) approach, as detailed in SI Results and Discussion, Genome Composition Analysis.

Fig. 2.

Schematic drawing of selected pathways of Polynucleobacter necessarius metabolism as inferred by genomic analysis. Elements in red are exclusive to the free-living strain’s genome. DH, dehydrogenase; cyt, cytochrome.

Fig. 3.

Nonsynonymous divergence between 904 homolog functional genes in the free-living and symbiotic Polynucleobacter necessarius. The rate of divergence from the outgroup is higher in the symbiont (averages: 0.0556, SE: 0.0049 vs. 0.0479, SE: 0.0035; P = 0.006, two-tailed t test). Axes are in logarithmic scale, and each circle represents the average position of 40 gene-windows projected onto the diagonal.