Genetic exchange shapes ultra-small Patescibacteria metabolic capacities in the terrestrial subsurface.

Abstract

Bacterial genomes are highly dynamic entities, mostly due to horizontal gene transfer (HGT). HGT is thought to be the main driver of genetic variation and adaptation to the local environment in bacteria. However, little is known about the modalities of HGT within natural microbial communities, especially the implications of genetic exchange for streamlined microorganisms such as Patescibacteria (Candidate Phyla Radiation). We searched for evidence of genetic exchange in 125 Patescibacteria genomes recovered from aquifer environments and detected the presence of hundreds of genomic islands, individually transferred genes, and prophages combined, with up to 13% of genome length attributed to HGT. Results show that most individual gene transfer events occurred between Patescibacteria, although putative donors included phylogenetically diverse groundwater microorganisms. For example, results indicate exchange of a lysR transcriptional regulator gene between Omnitrophota and Patescibacteria taxa with highly similar relative abundance patterns across 16 groundwater samples. Overall, results indicate a wide variety of metabolic functions were introduced into Patescibacteria genomes by HGT, including transcription, translation, and DNA replication, recombination and repair. This study illustrates the evolutionarily dynamic nature of Patescibacteria genomes despite the constraints of streamlining and that HGT in these organisms is also mediated via viral infection.

Importance: Genomic fluidity and diversity in bacteria are mainly governed by horizontal gene transfer (HGT), leading to a variety of genome structures and physiological diversity. The predominantly uncultivated Patescibacteria comprise highly diverse bacteria that consistently exhibit small cell and genome sizes. Despite strong pressures to reduce genetic content, we predict that these ultra-small bacteria use HGT to the same extent as other bacteria and that HGT may help facilitate recovery and maintenance of critical metabolic functions, niche exploitation, and putative symbiont-host interactions. Here, we determine the contribution of gene exchange to the evolution and diversification of Patescibacteria, despite the constraints of streamlining. We provide evidence of gene gains in Patescibacteria genomes recovered from aquifer environments and describe the large extent to which ultra-small bacterial genomes are subjected to HGT. Results suggest distinct metabolic functions acquired by Patescibacteria compared to general groundwater communities, suggesting specific evolutionary pressures on gene transfer dynamics occurring in ultra-small prokaryotes.