Comparative genomics of the carmine cochineal symbiont Candidatus Dactylopiibacterium carminicum reveals possible protection to the host against viruses via CRISPR/Cas

• Published in: Systematic and applied microbiology 2024-09, Vol.47 (5), p.126540, Article 126540
• Main Authors: Bustamante-Brito, Rafael, Vera-Ponce de León, Arturo, Rosenblueth, Mónica, Martínez-Romero, Esperanza
• Format: Article
• Language: English
• Subjects: Beta-proteobacteria; Comparative genomics; CRISPR; Insect symbiosis; Nitrogen fixation; Nucleopolyhedrovirus
• ISSN: 0723-2020; 1618-0984; 1618-0984
• DOI: 10.1016/j.syapm.2024.126540

•Wild and domesticated Dactylopius cochineals produce pigments with commercial value in the dye industry.•We found a nitrogen-fixing bacterium Candidatus Dactylopiibacterium carminicum in all microbiomes from wild and domesticated cochineals from the insect hemolymph, guts and ovaries.•Metagenome assembled genomes (MAGs) from wild and domesticated cochineals had ANIs over 98% showing a high genome conservation in all dactylopiibacteria. Genome comparisons allowed the metabolic reconstruction of Candidatus Dactylopiibacterium carminicum revealing a nutritional role.•We discovered CRISPRs in all dactylopiibacterial genomes that have a spacer that matches an insect virus and propose a defensive role of this bacterial symbiosis. We present new genomes from the bacterial symbiont Candidatus Dactylopiibacterium carminicum obtained from non-domesticated carmine cochineals belonging to the scale insect Dactylopius (Hemiptera: Coccoidea: Dactylopiidae). As Dactylopiibacterium has not yet been cultured in the laboratory, metagenomes and metatranscriptomics have been key in revealing putative symbiont functions. Dactylopiibacterium is a nitrogen-fixing beta-proteobacterium that may be vertically transmitted and shows differential gene expression inside the cochineal depending on the tissue colonized. Here we found that all cochineal species tested had Dactylopiibacterium carminicum which has a highly conserved genome. All Dactylopiibacterium genomes analyzed had genes involved in nitrogen fixation and plant polymer degradation. Dactylopiibacterium genomes resemble those from free-living plant bacteria, some found as endophytes. Notably, we found here a new putative novel function where the bacteria may protect the insect from viruses, since all Dactylopiibacterium genomes contain CRISPRs with a spacer matching nucleopolyhedrovirus that affects insects.