Specificities and functional coordination between the two Cas6 maturation endonucleases in Anabaena sp. PCC 7120 assign orphan CRISPR arrays to three groups

References

• Hille F, Richter H, Wong SP, et al. The biology of CRISPR-Cas: backward and forward. Cell. 2018;172:1239–1259.
   PubMed Web of Science ®Google Scholar
• Makarova KS, Wolf YI, Iranzo J, et al. Evolutionary classification of CRISPR-Cas systems: a burst of class 2 and derived variants. Nat Rev Microbiol. 2020;18:67–83.
   PubMed Web of Science ®Google Scholar
• Westra ER, Dowling AJ, Broniewski JM, et al. Evolution and ecology of CRISPR. Annu Rev Ecol Evol Syst. 2016;47:307–331.
   Web of Science ®Google Scholar
• Charpentier E, Richter H, van der Oost J, et al. Biogenesis pathways of RNA guides in archaeal and bacterial CRISPR-Cas adaptive immunity. FEMS Microbiol Rev. 2015;39:428–441.
   PubMed Web of Science ®Google Scholar
• Hochstrasser ML, Doudna JA. Cutting it close: CRISPR-associated endoribonuclease structure and function. Trends Biochem Sci. 2015;40:58–66.
   PubMed Web of Science ®Google Scholar
• Behler J, Hess WR. Approaches to study CRISPR RNA biogenesis and the key players involved. Methods. 2019;172:12–26.
   PubMed Web of Science ®Google Scholar
• Hale C, Kleppe K, Terns RM, et al. Prokaryotic silencing (psi)RNAs in Pyrococcus furiosus. RNA. 2008;14:2572–2579.
   PubMed Web of Science ®Google Scholar
• Hale CR, Zhao P, Olson S, et al. RNA-guided RNA cleavage by a CRISPR RNA-Cas protein complex. Cell. 2009;139:945–956.
   PubMed Web of Science ®Google Scholar
• Karginov FV, Hannon GJ. The CRISPR system: small RNA-guided defense in Bacteria and Archaea. Mol Cell. 2010;37:7–19.
   PubMed Web of Science ®Google Scholar
• Przybilski R, Richter C, Gristwood T, et al. Csy4 is responsible for CRISPR RNA processing in Pectobacterium atrosepticum. RNA Biol. 2011;8:517–528.
   PubMed Web of Science ®Google Scholar
• Carte J, Wang R, Li H, et al. Cas6 is an endoribonuclease that generates guide RNAs for invader defense in prokaryotes. Genes Dev. 2008;22:3489–3496.
   PubMed Web of Science ®Google Scholar
• Behler J, Sharma K, Reimann V, et al. The host-encoded RNase E endonuclease as the crRNA maturation enzyme in a CRISPR–Cas subtype III-Bv system. Nat Microbiol. 2018;3:367–377.
   PubMed Web of Science ®Google Scholar
• Chou-Zheng L, Hatoum-Aslan A. A type III-A CRISPR-Cas system employs degradosome nucleases to ensure robust immunity. Elife. 2019;8:e45393.
   PubMed Web of Science ®Google Scholar
• Hou S, Brenes-Álvarez M, Reimann V, et al. CRISPR-Cas systems in multicellular cyanobacteria. RNA Biol. 2019;16:518–529.
   PubMed Web of Science ®Google Scholar
• Makarova KS, Wolf YI, Alkhnbashi OS, et al. An updated evolutionary classification of CRISPR-Cas systems. Nat Rev Microbiol. 2015;13:722–736.
   PubMed Web of Science ®Google Scholar
• Zhang Q, Ye Y. Not all predicted CRISPR–Cas systems are equal: isolated cas genes and classes of CRISPR like elements. BMC Bioinformatics. 2017;18:92.
   PubMed Web of Science ®Google Scholar
• Strecker J, Ladha A, Gardner Z, et al. RNA-guided DNA insertion with CRISPR-associated transposases. Science. 2019;365:48–53.
   PubMed Web of Science ®Google Scholar
• Shah SA, Alkhnbashi OS, Behler J, et al. Comprehensive search for accessory proteins encoded with archaeal and bacterial type III CRISPR-cas gene cassettes reveals 39 new cas gene families. RNA Biol. 2019;16:530–542.
   PubMed Web of Science ®Google Scholar
• Chénard C, Wirth JF, Suttle CA. Viruses infecting a freshwater filamentous Cyanobacterium (Nostoc sp.) encode a functional CRISPR array and a proteobacterial DNA polymerase B. MBio. 2016;7:e00667–16.
   PubMed Web of Science ®Google Scholar
• Adolph KW, Haselkorn R. Isolation and characterization of a virus infecting the blue-green alga Nostoc muscorum. Virology. 1971;46:200–208.
   PubMed Web of Science ®Google Scholar
• Adolph KW, Haselkorn R. Blue-green algal virus N-1: physical properties and disassembly into structural parts. Virology. 1973;53:427–440.
   PubMed Web of Science ®Google Scholar
• Rippka R, Deruelles J, Waterbury JB, et al. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Microbiology. 1979;111:1–61.
   Web of Science ®Google Scholar
• Ungerer J, Pakrasi HB. Cpf1 is a versatile tool for CRISPR genome editing across diverse species of Cyanobacteria. Sci Rep. 2016;6:39681.
   PubMed Web of Science ®Google Scholar
• Elhai J, Wolk CP. Conjugal transfer of DNA to cyanobacteria. Meth Enzymol. 1988;167:747–754.
   PubMed Web of Science ®Google Scholar
• Pinto FL, Thapper A, Sontheim W, et al. Analysis of current and alternative phenol based RNA extraction methodologies for cyanobacteria. BMC Mol Biol. 2009;10:79.
   PubMed Web of Science ®Google Scholar
• Steglich C, Futschik ME, Lindell D, et al. The challenge of rRegulation in a minimal photoautotroph: non-coding RNAs in Prochlorococcus. PLoS Genet. 2008;4:e1000173.
   PubMed Web of Science ®Google Scholar
• Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal. 2011;17:10.
   Google Scholar
• Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357–359.
   PubMed Web of Science ®Google Scholar
• Maxwell CS, Jacobsen T, Marshall R, et al. A detailed cell-free transcription-translation-based assay to decipher CRISPR protospacer-adjacent motifs. Methods. 2018;143:48–57.
   PubMed Web of Science ®Google Scholar
• Shin J, Noireaux V. An E. coli cell-free expression toolbox: application to synthetic gene circuits and artificial cells. ACS Synth Biol. 2012;1:29–41.
   PubMed Web of Science ®Google Scholar
• Zimmermann L, Stephens A, Nam S-Z, et al. A completely reimplemented MPI bioinformatics toolkit with a new HHpred server at its core. J Mol Biol. 2018;430:2237–2243.
   PubMed Web of Science ®Google Scholar
• Reimann V, Alkhnbashi OS, Saunders SJ, et al. Structural constraints and enzymatic promiscuity in the Cas6-dependent generation of crRNAs. Nucleic Acids Res. 2017;45:915–925.
   PubMed Web of Science ®Google Scholar
• Almendros C, Nobrega FL, McKenzie RE, et al. Cas4-Cas1 fusions drive efficient PAM selection and control CRISPR adaptation. Nucleic Acids Res. 2019;47:5223–5230.
   PubMed Web of Science ®Google Scholar
• Marchler-Bauer A, Bo Y, Han L, et al. CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res. 2017;45:D200–3.
   PubMed Web of Science ®Google Scholar
• Oliveira P, Martins NM, Santos M, et al. The Anabaena sp. PCC 7120 exoproteome: taking a peek outside the box. Life (Basel). 2015;5:130–163.
   PubMedGoogle Scholar
• Raden M, Ali SM, Alkhnbashi OS, et al. Freiburg RNA tools: a central online resource for RNA-focused research and teaching. Nucleic Acids Res. 2018;46:W25–9.
   PubMed Web of Science ®Google Scholar
• Will S, Joshi T, Hofacker IL, et al. LocARNA-P: accurate boundary prediction and improved detection of structural RNAs. RNA. 2012;18:900–914.
   PubMed Web of Science ®Google Scholar
• Majumdar S, Zhao P, Pfister NT, et al. Three CRISPR-Cas immune effector complexes coexist in Pyrococcus furiosus. RNA. 2015;21:1147–1158.
   PubMed Web of Science ®Google Scholar
• Nickel L, Weidenbach K, Jäger D, et al. Two CRISPR-Cas systems in Methanosarcina mazei strain Gö1 display common processing features despite belonging to different types I and III. RNA Biol. 2013;10:779–791.
   PubMed Web of Science ®Google Scholar
• Nickel L, Ulbricht A, Alkhnbashi OS, et al. Cross-cleavage activity of Cas6b in crRNA processing of two different CRISPR-Cas systems in Methanosarcina mazei Gö1. RNA Biol. 2019;16:492–503.
   PubMed Web of Science ®Google Scholar
• He F, Bhoobalan-Chitty Y, Van LB, et al. Anti-CRISPR proteins encoded by archaeal lytic viruses inhibit subtype I-D immunity. Nat Microbiol. 2018;3:461–469.
   PubMed Web of Science ®Google Scholar
• Gussow AB, Shmakov SA, Makarova KS, et al. Vast diversity of anti-CRISPR proteins predicted with a machine-learning approach. bioRxiv. 2020. DOI:2020.01.23.916767.
   PubMedGoogle Scholar
• Kumar S, Stecher G, Li M, et al. Genetics Analysis across computing platforms. Mol Biol Evol. 2018;35:1547–1549.
   PubMed Web of Science ®Google Scholar
• Rzhetsky A, Nei M. A simple method for estimating and testing minimum evolution trees. Mol Biol Evol. 1992;9:945–967.
   Web of Science ®Google Scholar
• Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution. 1985;39:783–791.
   PubMed Web of Science ®Google Scholar
• Zuckerkandl E, Pauling L. Evolutionary divergence and convergence in proteins. In: Bryson V, Vogel HJ, editors. Evolving Genes and Proteins. New York, NY: Academic Press; 1965. p. 97–166.
   Google Scholar
• Nei M, Kumar S. Molecular Evolution and Phylogenetics. New York, NY: Oxford University Press; 2000.
   Google Scholar
• Saitou N, Nei M. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4:406–425.
   PubMed Web of Science ®Google Scholar