The Rare Plasmid Biosphere: A Hidden Reservoir of Genetic Diversity

Abstract

Bacterial communities typically display highly uneven abundance patterns, with a few dominant taxa and many low-abundance ones contributing to extensive genetic diversity 1-4. Notably, this rare biosphere 5 includes species performing critical ecological functions, such as biogeochemical cycling and resisting invasions 6-9. While bacterial abundance patterns have been extensively studied, the distribution of plasmids-extrachromosomal, self-replicating genetic elements ubiquitous in prokaryotes-- remains poorly understood. Using a dataset of 52,909 plasmids from isolates of bacteria and archaea 10, we found that their 16,547 Plasmid Taxonomic Units (PTUs) 11,12 exhibit a distribution with a fat tail, whether in rank abundance or relative abundance distributions: a few highly prevalent PTUs and many rare. The relative abundance distributions are well described by a Poisson log-normal distribution, consistent with recent findings for species abundance distributions across several taxonomic groups 13. The host distribution also presents a heavy tail; however, we show that rare PTUs are not necessarily associated with rare bacterial species, nor are common PTUs exclusively found in common hosts. This indicates that PTUs distribution is not a direct consequence of hosts distribution. Per plasmid, the host range of rare PTUs is higher than that of common PTUs, at all taxa levels, from species to phyla. Yet, plasmids from common PTUs are more mobile, likely explaining their success. The large group of rare PTUs constitutes a much more diverse reservoir of genetic material than the group of common PTUs. Under appropriate selective pressures, some of these rare plasmids could spread not only by hitchhiking with their hosts but also through horizontal transfer. Therefore, this work opens new paths into plasmid research.