TY - JOUR
T1 - Retroelement-guided protein diversification abounds in vast lineages of Bacteria and Archaea
AU - Paul, Blair G.
AU - Burstein, David
AU - Castelle, Cindy J.
AU - Handa, Sumit
AU - Arambula, Diego
AU - Czornyj, Elizabeth
AU - Thomas, Brian C.
AU - Ghosh, Partho
AU - Miller, Jeff F.
AU - Banfield, Jillian F.
AU - Valentine, David L.
N1 - Funding Information:
This research was funded by National Science Foundation grant no. OCE-1046144 to D.L.V., National Institutes of Health grant no. R01 AI096838 to J.F.M. and P.G., and by the US Department of Energy (DOE), Office of Science, Office of Biological and Environmental Research under award no. DE-AC02-05CH11231 (Sustainable Systems Scientific Focus Area; Lawrence Berkley National Laboratory operated by the University of California) and award no. DE-SC0004918 (Systems Biology Knowledge Base Focus Area). Sequencing was performed at the US DOE Joint Genome Institute, a DOE Office of Science User Facility, supported under contract no. DE-AC02-05CH11231. Metatranscriptomes were sequenced at the DOE-supported Environmental Molecular Sciences Laboratory at Pacific Northwest National Laboratory. B.G.P. was supported by a postdoctoral fellowship from the Center for Dark Energy Biosphere Investigations (C-DEBI). D.B. was supported by a long-term EMBO fellowship. The authors thank K. Anantharaman for assistance with genome binning, A. Singh and C.T. Brown, who aided in examining CPR and DPANN genomes and C. Magnabosco for offering insights on phylogenetic reconstruction. This is C-DEBI contribution no. 361.
Publisher Copyright:
© 2017 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
PY - 2017/6
Y1 - 2017/6
N2 - Major radiations of enigmatic Bacteria and Archaea with large inventories of uncharacterized proteins are a striking feature of the Tree of Life 1-5. 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 hypervariability 6-8, 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.
AB - Major radiations of enigmatic Bacteria and Archaea with large inventories of uncharacterized proteins are a striking feature of the Tree of Life 1-5. 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 hypervariability 6-8, 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.
UR - https://www.scopus.com/pages/publications/85017034268
U2 - 10.1038/nmicrobiol.2017.45
DO - 10.1038/nmicrobiol.2017.45
M3 - Article
C2 - 28368387
AN - SCOPUS:85017034268
SN - 2058-5276
VL - 2
JO - Nature Microbiology
JF - Nature Microbiology
M1 - 17045
ER -