title: Retroelement-guided protein diversification abounds in vast lineages of Bacteria and Archaea.
abstract: Major radiations of enigmatic Bacteria and Archaea with large inventories of uncharacterized proteins are a striking feature of the Tree of Life1-5. 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 hypervariability6-8, 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.
authors.affiliation: Marine Science Institute, University of California, Santa Barbara, California 93106, USA.
authors.forename: Blair G
authors.initials: BG
authors.lastname: Paul
authors.affiliation: Department of Earth and Planetary Science, University of California, Berkeley, California 94720, USA.
authors.forename: David
authors.initials: D
authors.lastname: Burstein
authors.affiliation: Department of Earth and Planetary Science, University of California, Berkeley, California 94720, USA.
authors.forename: Cindy J
authors.initials: CJ
authors.lastname: Castelle
authors.affiliation: Department of Chemistry and Biochemistry, UC San Diego, La Jolla, California 92093, USA.
authors.forename: Sumit
authors.initials: S
authors.lastname: Handa
authors.affiliation: Department of Microbiology, Immunology and Molecular Genetics, University of California, Los Angeles, California 90095, USA.
authors.forename: Diego
authors.initials: D
authors.lastname: Arambula
authors.affiliation: Department of Microbiology, Immunology and Molecular Genetics, University of California, Los Angeles, California 90095, USA.
authors.forename: Elizabeth
authors.initials: E
authors.lastname: Czornyj
authors.affiliation: Department of Earth and Planetary Science, University of California, Berkeley, California 94720, USA.
authors.forename: Brian C
authors.initials: BC
authors.lastname: Thomas
authors.affiliation: Department of Chemistry and Biochemistry, UC San Diego, La Jolla, California 92093, USA.
authors.forename: Partho
authors.initials: P
authors.lastname: Ghosh
authors.affiliation: Department of Microbiology, Immunology and Molecular Genetics, University of California, Los Angeles, California 90095, USA.|Molecular Biology Institute, University of California, Los Angeles, California 90095, USA.|California NanoSystems Institute, University of California, Los Angeles, California 90095, USA.
authors.forename: Jeff F
authors.initials: JF
authors.lastname: Miller
authors.affiliation: Department of Earth and Planetary Science, University of California, Berkeley, California 94720, USA.|Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA.|Department of Environmental Science, Policy, and Management, University of California, Berkeley, California 94720, USA.
authors.forename: Jillian F
authors.initials: JF
authors.lastname: Banfield
authors.affiliation: Marine Science Institute, University of California, Santa Barbara, California 93106, USA.|Department of Earth Science, UC Santa Barbara, Santa Barbara, California 93106 USA.
authors.forename: David L
authors.identifier: http://orcid.org/0000-0001-5914-9107
authors.initials: DL
authors.lastname: Valentine
mesh_terms: D001105:Archaea / Q000145:classification / Q000235:genetics* / Q000378:metabolism; D019843:Archaeal Proteins / Q000235:genetics*; D001419:Bacteria / Q000145:classification / Q000235:genetics* / Q000378:metabolism; D001426:Bacterial Proteins / Q000235:genetics*; D019143:Evolution, Molecular; D020745:Genome, Archaeal; D016680:Genome, Bacterial; D023281:Genomics; D046588:Nanoarchaeota / Q000235:genetics / Q000378:metabolism; D010802:Phylogeny; D012194:RNA-Directed DNA Polymerase / Q000235:genetics; D018626:Retroelements / Q000235:genetics*
chemical_list: D019843:Archaeal Proteins; D001426:Bacterial Proteins; D018626:Retroelements; D012194:RNA-Directed DNA Polymerase