Abstract
The CRISPR-Cas system is widely distributed in prokaryotes and plays an important role in the adaptive immunity of bacteria and archaea. Bifidobacterium is an important component of the intestinal flora of humans and animals, and some species of this bacterium can be employed as food additives. However, the Bifidobacterium CRISPR-Cas system has not been fully elucidated to date. In this study, the genomes of 110 strains of Bifidobacterium were employed to research the diversity of the type I-U system. The 110 strains were divided into five groups according to the genes adjacent to the CRISPR locus, including group A, B, C, D and E. Strains in the intergroup had unique species classifications and MLST types. An evolutionary tree was constructed based on the conserved cas4/cas1 fusion gene. The results showed that group A had a different evolutionary branch compared with the other groups and had a relatively low spacer number. Notably, group B, C and E had exhibited ABC transporter regulators in the genes adjacent to the CRISPR locus. ABC transporters play important roles in the exocytosis of many antibiotics and are involved in horizontal gene transfer. This mechanism may have promoted the evolution of Bifidobacterium and the horizontal gene transfer of the type I-U system, which may have promoted the generation of system diversity. In summary, our results help to elucidate the role of the type I-U system in the evolution of Bifidobacterium.
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References
Aggarwala V, Liang G, Bushman FD (2017) Viral communities of the human gut: metagenomic analysis of composition and dynamics. Mob DNA 8:12
Almendros C, Nobrega FL, McKenzie RE, Brouns SJJ (2019) Cas4-Cas1 fusions drive efficient PAM selection and control CRISPR adaptation. Nucleic Acids Res 47:5223–5230
Barrangou R (2015) The roles of CRISPR-Cas systems in adaptive immunity and beyond. Curr Opin Immunol 32:36–41
Barrangou R et al (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:1709–1712
Biswas A, Gagnon JN, Brouns SJ, Fineran PC, Brown CM (2013) CRISPR Target: bioinformatic prediction and analysis of crRNA targets. RNA Biol 10:817–827
Briner AE et al (2015) Occurrence and diversity of CRISPR-Cas systems in the genus bifidobacterium. PLoS One 10:e0133661
Bunesova V et al (2017) Diversity of the subspecies Bifidobacterium animalis subsp. lactis. Anaerobe 44:40–47
Chouraqui JP, Van Egroo LD, Fichot MC (2004) Acidified milk formula supplemented with bifidobacterium lactis: impact on infant diarrhea in residential care settings. J Pediatr Gastroenterol Nutr 38:288–292
Couvin D et al (2018) CRISPR Cas Finder, an update of CRISR Finder, includes a portable version, enhanced performance and integrates search for Cas proteins. Nucleic Acids Res 46:W246-w251
Cronin M, Ventura M, Fitzgerald GF, van Sinderen D (2011) Progress in genomics, metabolism and biotechnology of bifidobacteria. Int J Food Microbiol 149:4–18
Deveau H, Garneau JE, Moineau S (2010) CRISPR/Cas system and its role in phage-bacteria interactions. Annu Rev Microbiol 64:475–493
Du D et al (2018) Multidrug efflux pumps: structure, function and regulation. Nat Rev Microbiol 16:523–539
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. EvolInt J Org Evol 39:783–791
Fijan S (2014) Microorganisms with claimed probiotic properties: an overview of recent literature. Int J Environ Res Public Health 11:4745–4767
Frols S et al (2007) Response of the hyperthermophilic archaeon Sulfolobus solfataricus to UV damage. J Bacteriol 189:8708–8718
Garneau JE et al (2010) The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468:67–71
Gootenberg JS et al (2017) Nucleic acid detection with CRISPR-Cas13a/C2c2. Science 356:438–442
Grissa I, Vergnaud G, Pourcel C (2007) The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats. BMC Bioinform 8:172
He T et al (2008) Effects of yogurt and bifidobacteria supplementation on the colonic microbiota in lactose-intolerant subjects. J Appl Microbiol 104:595–604
Hidalgo-Cantabrana C, Crawley AB, Sanchez B, Barrangou R (2017) Characterization and exploitation of CRISPR loci in Bifidobacterium longum. Front Microbiol 8:1851
Ishino Y, Shinagawa H, Makino K, Amemura M, Nakata A (1987) Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product. J Bacteriol 169:5429–5433
Killer J, Sedlacek I, KopecnyJ Reclassification of Bifidobacterium stercoris Kim, et al (2013) 2010 as a later heterotypic synonym of Bifidobacterium adolescentis. Int J Syst Evol Microbiol 63:4350–4353
Koonin EV, Makarova KS, Zhang F (2017) Diversity, classification and evolution of CRISPR-Cas systems. Curr Opin Microbiol 37:67–78
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549
Le Leu RK, Hu Y, Brown IL, Woodman RJ, Young GP (2010) Synbiotic intervention of Bifidobacterium lactis and resistant starch protects against colorectal cancer development in rats. Carcinogenesis 31:246–251
Li M, Wang R, Zhao D, Xiang H (2014) Adaptation of the Haloarcula hispanica CRISPR-Cas system to a purified virus strictly requires a priming process. Nucleic Acids Res 42:2483–2492
Lurie-Weinberger MN, Peeri M, Tuller T, Gophna U (2012) Extensive inter-domain lateral gene transfer in the evolution of the human commensal methano sphaerastadtmanae. Front Genet 3:182
Makarova KS et al (2011) Evolution and classification of the CRISPR-Cas systems. Nat Rev Microbiol 9:467–477
Makarova KS et al (2015) An updated evolutionary classification of CRISPR-Cas systems. Nat Rev Microbiol 13:722–736
Makino H et al (2011) Transmission of intestinal Bifidobacterium longum subsp. longum strains from mother to infant, determined by multilocus sequencing typing and amplified fragment length polymorphism. Appl Environ Microbiol 77:6788–6793
Marraffini LA, Sontheimer EJ (2010) CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea. Nat Rev Genet 11:181–190
Meehan CJ, Beiko RG (2012) Lateral gene transfer of an ABC transporter complex between major constituents of the human gut microbiome. BMC Microbiol 12:248
Milani C et al (2013) Comparative genomics of Bifidobacterium animalis subsp. lactis reveals a strict monophyletic bifidobacterial taxon. Appl Environ Microbiol 79:4304–4315
Miryala SK, Ramaiah S (2019) Exploring the multi-drug resistance in Escherichia coli O157:H7 by gene interaction network: a systems biology approach. Genomics 111:958–965
Nethery MA, Barrangou R (2019) CRISPR visualizer: rapid identification and visualization of CRISPR loci via an automated high-throughput processing pipeline. RNA Biol 16:577–584
Nilsson E et al (2019) Genomic and seasonal variations among aquatic phages infecting the Baltic Sea gamma proteo bacterium sp. strain BAL341. Appl Environ Microbiol. https://doi.org/10.1128/AEM.01003-19
Nuñez JK, Kranzusch PJ, Noeske J, Wright AV, Davies CW, Doudna JA (2014) Cas1-Cas2 complex formation mediates spacer acquisition during CRISPR-Cas adaptive immunity. Nat Struct Mol Biol 21:528–534
Ohtani K, Shimizu T (2016) Regulation of toxin production in Clostridium perfringens. Toxins (Basel) 8:1–14
Pan M, Nethery MA, Hidalgo-Cantabrana C, Barrangou R (2020) Comprehensive mining and characterization of CRISPR-Cas systems in Bifidobacterium. Microorganisms 8:1–18
Panta PR et al (2019) A DedA family membrane protein is required for colistin resistance. Front Microbiol 10:2532
Pereira DI, Gibson GR (2002) Effects of consumption of probiotics and prebiotics on serum lipid levels in humans. Crit Rev Biochem Mol Biol 37:259–281
Plagens A, Tjaden B, Hagemann A, Randau L, Hensel R (2012) Characterization of the CRISPR/Cas subtype I-A system of the hyperthermophilic Crenarchaeon Thermoproteus tenax. J Bacteriol 194:2491–2500
Rahman SJ, Kaur P (2018) Conformational changes in a multidrug resistance ABC transporter DrrAB: fluorescence-based approaches to study substrate binding. Arch Biochem Biophys 658:31–45
Richter C, Gristwood T, Clulow JS, Fineran PC (2012) In vivo protein interactions and complex formation in the Pectobacterium atrosepticum subtype I-F CRISPR/Cas system. PLoS One 7:e49549
Saavedra JM, Bauman NA, Oung I, Perman JA, Yolken RH (1994) Feeding of Bifidobacterium bifidum and Streptococcus thermophilus to infants in hospital for prevention of diarrhoea and shedding of rotavirus. Lancet 344:1046–1049
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Shariat N, Sandt CH, DiMarzio MJ, Barrangou R, Dudley EG (2013) CRISPR MVLST subtyping of Salmonella enterica subsp. entericaserovars Typhimurium and Heidelberg and application in identifying outbreak isolates. BMC Microbiol 13(254):1–17
Shkoporov AN et al (2019) The human gut virome is highly diverse stable and individual specific. Cell Host Microbe 26(4):527–541
Silva AM, Barbosa FH, Duarte R, Vieira LQ, Arantes RM, Nicoli JR (2004) Effect of Bifidobacterium longum ingestion on experimental salmonellosis in mice. J Appl Microbiol 97:29–37
Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577
Tang K, Huang H, Jiao N, Wu CH (2010) Phylogenomic analysis of marine Roseobacters. PLoS One 5:e11604
Tanigawa K, Watanabe K (2011) Multilocus sequence typing reveals a novel subspeciation of Lactobacillus delbrueckii. Microbiology 157:727–738
Ventura M et al (2006) Analysis of bifidobacterial evolution using a multilocus approach. Int J Syst Evol Microbiol 56:2783–2792
Vestergaard G, Garrett RA, Shah SA (2014) CRISPR adaptive immune systems of Archaea. RNA Biol 11:156–167
Westra ER, Buckling A, Fineran PC (2014) CRISPR-Cas systems: beyond adaptive immunity. Nat Rev Microbiol 12:317–326
Xue W et al (2014) CRISPR-mediated direct mutation of cancer genes in the mouse liver. Nature 514:380–384
Zhang J, Kasciukovic T, White MF (2012) The CRISPR associated protein Cas4 Is a 5’ to 3’ DNA exonuclease with an iron-sulfur cluster. PLoS One 7:e47232
Funding
The work was funded by the National Science and Technology Specific Projects (2018ZX10301407), the Key Scientific Research Project of Colleges and Universities in Henan Province (Grant No. 20A330004) and the National Natural Science Foundation of China (Grant No. 81573205).
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LO, GD and SC designed the study, and LO, JL and YT analyzed the data and wrote the paper. HY and YX collected some data. All authors read and approved the final manuscript.
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Communicated by Erko Stackebrandt.
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Ou, L., Long, J., Teng, Y. et al. Diversity of the type I-U CRISPR-Cas system in Bifidobacterium. Arch Microbiol 203, 3235–3243 (2021). https://doi.org/10.1007/s00203-021-02310-w
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DOI: https://doi.org/10.1007/s00203-021-02310-w