Targeted hypermutation of putative antigen sensors in multicellular bacteria

• 成果类型: Article
• 署名作者: Dore, Hugo; Eisenberg, Amy R.; Junkins, Emily N.; Leventhal, Gabriel E.; Ganesh, Anakha; Cordero, Otto X.; Paul, Blair G.; Valentine, David L.; O'Malley, Michelle A.; Wilbanks, Elizabeth G.
• 署名单位: Ifremer; Universite de Bretagne Occidentale; University of California System; University of California Santa Barbara; University of California System; University of California Santa Barbara; Massachusetts Institute of Technology (MIT); Marine Biological Laboratory - Woods Hole; University of California System; University of California Santa Barbara; University of California System; University of California Santa Barbara; University of California System; University of California Santa Barbara; Marine Biological Laboratory - Woods Hole
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-11894
• DOI: 10.1073/pnas.2316469121
• 发表日期: 2024-02-27
• 关键词: diversity-generating retroelements; purple sulfur bacterium; gen. nov.; lectin fold; EVOLUTION; identification; performance; mechanisms; SEQUENCES; multiple

摘要

Diversity - generating retroelements (DGRs) are used by bacteria, archaea, and viruses as a targeted mutagenesis tool. Through error - prone reverse transcription, DGRs introduce random mutations at specific genomic loci, enabling rapid evolution of these targeted genes. However, the function and benefits of DGRdiversified proteins in cellular hosts remain elusive. We find that 82% of DGRs from one of the major monophyletic lineages of DGR reverse transcriptases are encoded by multicellular bacteria, which often have two or more DGR loci in their genomes. Using the multicellular purple sulfur bacterium Thiohalocapsa sp. PB - PSB1 as an example, we characterized nine distinct DGR loci capable of generating 10 282 different combinations of target proteins. With environmental metagenomes from individual Thiohalocapsa aggregates, we show that most of PB - PSB1's DGR target genes are diversified across its biogeographic range, with spatial heterogeneity in the diversity of each locus. In Thiohalocapsa PB - PSB1 and other bacteria hosting this lineage of cellular DGRs, the diversified target genes are associated with NACHT - domain anti - phage defenses and putative ternary conflict systems previously shown to be enriched in multicellular bacteria. We propose that these DGRdiversified targets act as antigen sensors that confer a form of adaptive immunity to their multicellular consortia, though this remains to be experimentally tested. These findings could have implications for understanding the evolution of multicellularity, as the NACHT - domain anti - phage systems and ternary systems share both domain homology and conceptual similarities with the innate immune and programmed cell death pathways of plants and metazoans.