Major radiations of enigmatic Bacteria and Archaea with large inventories of uncharacterized proteins are a striking feature of the Tree of Life The processes that led to functional diversity in these lineages, which may contribute to a host-dependent lifestyle, are poorly understood. Here, we show that diversity-generating retroelements (DGRs), which guide site-specific protein hypervariability, are prominent features of genomically reduced organisms from the bacterial candidate phyla radiation (CPR) and as yet uncultivated phyla belonging to the DPANN (Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota and Nanohaloarchaea) archaeal superphylum. From reconstructed genomes we have defined monophyletic bacterial and archaeal DGR lineages that expand the known DGR range by 120% and reveal a history of horizontal retroelement transfer. Retroelement-guided diversification is further shown to be active in current CPR and DPANN populations, with an assortment of protein targets potentially involved in attachment, defence and regulation. Based on observations of DGR abundance, function and evolutionary history, we find that targeted protein diversification is a pronounced trait of CPR and DPANN phyla compared to other bacterial and archaeal phyla. This diversification mechanism may provide CPR and DPANN organisms with a versatile tool that could be used for adaptation to a dynamic, host-dependent existence.
This fellowship was broadly aimed at examining accelerated protein evolution by microorganisms in subsurface environments. A variety of bacteria, archaea, and their viruses are capable of generating massive protein variation for specific genes, to a degree that is unparalleled in other forms of life, yet this phenomenon has not been investigated in the subsurface biosphere. A combination of molecular and bioinformatic techniques enabled identification of gene-diversifying elements across a multitude of microbial and viral genomes. Genomes bearing this trait were found in three subsurface systems: a terrestrial aquifer, coastal marine sediments, and subsurface crustal fluids. As a product of this fellowship, papers have been published describing the abundance and functional diversity of hypervariable genes in groundwater metagenomes, and, separately, on the structural characterization of a hypervariable protein from nanoarchaea. An additional manuscript is in preparation, which highlights the importance of localized hypermutation in manipulating host-parasite interactions for archaeal viruses from crustal fluids. Through new collaboration, research on this phenomenon has also extended beyond subsurface microorganisms, to address the importance of accelerated evolution in structuring host-microbe-virus interactions in the human microbiome.