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The Rich Repertoire of Antibiotic Resistance Genes in Candidate Phyla Radiation Genomes

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The Rich Repertoire of Antibiotic Resistance Genes in Candidate Phyla Radiation Genomes bioRxiv preprint doi: https://doi.org/10.1101/2021.07.02.450847; this version posted July 2, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Title: Small and equipped: the rich repertoire of antibiotic resistance genes in Candidate 2 Phyla Radiation genomes 3 Running title: Microbial competition: CPR are players 4 Authors list: Mohamad Maatouk1,2, Ahmad Ibrahim1,2, Jean-Marc Rolain1,2, Vicky 5 Merhej1,2*, Fadi Bittar1,2* 6 Affiliations : 1 Aix-Marseille Univ, IRD, APHM, MEPHI, 27 boulevard Jean Moulin, 13385 Marseille 7 CEDEX 05, France. 8 2IHU Méditerranée Infection, 19-21 boulevard Jean Moulin, 13385 Marseille CEDEX 05, France 9 * Corresponding author: Fadi Bittar. Email: [email protected]; ORCID: 0000-0003-4052- 10 344X. 11 Vicky Merhej. Email: [email protected] 12 13 14 15 Abstract: 256 words 16 Text: 4,005 words 17 Reference: 40 18 Figures: 5 figures and 2 supplementary figures 19 Tables: 1 supplementary table 20 21 22 1 bioRxiv preprint doi: https://doi.org/10.1101/2021.07.02.450847; this version posted July 2, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 23 ABSTRACT 24 Microbes belonging to Candidate Phyla Radiation (CPR) have joined the tree of life as a new 25 unique branch, thanks to the intensive application of metagenomics and advances of 26 sequencing technologies. Despite their ultra-small size, reduced genome and metabolic 27 pathways which mainly depend on symbiotic/exo-parasitic relationship with their bacterial 28 host, CPR microbes are abundant and ubiquitous in almost all environments and are 29 consequently survivors in highly competitive circumstances within microbial communities. 30 They have been eventually identified by 16S rRNA analysis and represent more than 26% of 31 microbial diversity. CPR microbes were able to survive in this context, although their defence 32 mechanisms and phenotypic characteristic remain, however, poorly explored. Here, we 33 conducted a thorough in-silico analysis on 4,062 CPR genomes to test whether these 34 ultrasmall microorganisms might encode for antibiotic resistance (AR)-like enzymes. We 35 used an adapted AR screening criteria with an exhaustive consensus database and 36 complementary steps conferring their resistance functions. We conclude by reporting the 37 surprising discovery of rich reservoir of divergent AR-like genes (n= 30,545 HITs, mean=7.5 38 HITs/genome [0-41] encoding for 89 AR enzymes, distributed across the 13 CPR phyla, and 39 associated with 14 different chemical classes of antimicrobials. However, most HITs found 40 (93.6%) were linked to glycopeptide, beta-lactams, macrolide-lincosamide-streptogramin, 41 tetracycline and aminoglycoside resistance. Moreover, a distinct AR profile was discerned 42 between the microgenomates group and Candidatus Parcubacteria, and between each of them 43 and other CPR phyla. CPR cells seem to be active players during microbial competitive 44 interactions and are well-equipped for the microbial combat in different habitats, supporting 45 their natural survival/persistence and continued existence. 46 2 bioRxiv preprint doi: https://doi.org/10.1101/2021.07.02.450847; this version posted July 2, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 47 Introduction 48 The increased use of exploring tools in the 21st century, such as high-throughput sequencing 49 and its wide application in metagenomics, has led to broadening access to genomic data of 50 uncultured microorganisms1. These previously unrecognized genomes have challenged the 51 classical view of the tree of life and have given rise to new divisions. Representatives of these 52 divisions have been moved out of the group of undiscovered living organisms (microbial dark 53 matter)2. Among these discoveries, many questions have been raised about a new group of 54 microbes which is close to bacteria,, but which is quite unique, referred to as Candidate Phyla 55 radiation or CPR3,4. 56 CPR is a group of highly distinct and abundant ultra-small microbes, which represents more 57 than 26% of known bacterial diversity2. These microbes are characterised by their reduced- 58 size genomes5 and the occurrence of a high percentage of unknown-function proteins6. 59 Recently, a comparative study of protein families between CPR and bacteria showed that CPR 60 have a prevalence of proteins involved in a symbiotic lifestyle and interaction with other 61 microbes6,7.Therefore, they are highly auxotrophic with a lack of essential encoding genes for 62 some pathways which are critical to the autonomous lifestyle8. 63 Paradoxically, the lack of these genes can sometimes help them to survive in their habitat. For 64 example, despite the absence of a viral CRISPR defence system in Patescibacteria (the 65 phylum that contains most CPR genomes), members of this superphylum can escape 66 bacteriophage attacks (attachment) by the natural suppression of common phage membrane 67 receptors9. 68 However, these as yet uncultured microbes have been detected based on metagenomic or 69 metabarcoding analyses of ribosomal RNA sequences3. To date, CPR microbes have been 3 bioRxiv preprint doi: https://doi.org/10.1101/2021.07.02.450847; this version posted July 2, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 70 reported in different human microbiomes (buccal cavity, gut microbiota, vagina 71 etc.)10,11,12,13,14, as well as in the environment (soil, seawater, deep-sea sediments, termite guts 72 etc.)15,16,17,18,19,20. Their ubiquitous presence in complex ecosystems therefore suggests their 73 continuous competitive lifestyle against different microorganisms. This focusses attention on 74 understanding the defensive mechanisms employed by CPR microbes in habitats shared with 75 other microbes. 76 Moreover, according to metagenomic analyses of ancient DNA, CPR microbes have been 77 reported in ancient samples of Neanderthal calcified dental plaque (calculus) dated thousands 78 of years ago21. Like CPR, antibiotic resistance (AR) is an ancient phenomenon highly 79 reported in the microbial world22,23. Various studies have shown the natural existence of AR 80 genes in micro-organisms even before the discovery and introduction of antibiotics by 81 humans in the mid-twentieth century24. These AR genes have also been detected from ancient 82 samples dating back millions of years in diverse environments24. The mechanisms of AR are 83 due to the absence of antibiotic targets, their modification following a mutation on pre- 84 existing genes, or to the presence of protein coding genes25. Some genes can inactivate the 85 antibiotic by enzymatic activity, while other genes confer AR by target protection or 86 alteration25. 87 Given that CPR members (i) are widely spread in different ecological niches and 88 microbiomes, (ii) have never been isolated and grown in pure culture, and (iii) have a high 89 number of unknown biosynthetic activities within their genomes, few, if any studies have 90 looked into the defence mechanisms and competing behaviour of CPR cells. In fact, survival 91 strategies, which are pointedly AR gene components expressed by CPR members against 92 other microbes in different hostile/competitive environments, have not yet been explored. For 93 this propose, we describe the first repertoire of AR genes in CPR genomes by in silico 4 bioRxiv preprint doi: https://doi.org/10.1101/2021.07.02.450847; this version posted July 2, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 94 analysis, after developing suitable AR screening criteria. We found that CPR members are 95 also players in this microbial “infinity war”. 96 Materials and Methods 97 Genomic data: 98 For this study, all nucleotide sequences of CPR genomes available on 12 September 2020 on 99 the NCBI website (National Center for Biotechnology Information) 100 (https://www.ncbi.nlm.nih.gov) were selected and downloaded from the NCBI-GenBank 101 database. Genomes were chosen based on the taxonomy provided by the NCBI. The 4,062 102 CPR genomes are distributed across 2,222 Candidatus Parcubacteria, 933 Candidatus 103 Microgenomates, 284 Candidatus Saccharibacteria, 155 unclassified Patescibacteria group, 104 136 Candidate division WWE3 (Katanobacteria), 126 Candidatus Peregrinibacteria, 55 105 Candidatus Berkelbacteria, 53 Candidatus Dojkabacteria, 39 Candidatus Doudnabacteria, 33 106 Candidatus Gracilibacteria, 13 Candidatus Absconditabacteria, 11 Candidate division Kazan- 107 3B-28 and two Candidatus Wirthbacteria. Only 35 of all the genomes analysed were complete 108 genomes, while the remaining were whole genome sequences (WGS). 109 Genome annotation was generated using the Rapid Annotation using Subsystem Technology 110 tool kit (RASTtk)26 as implemented in the PATRIC v3.6.8 annotation web service. 111 Detection of Antibiotic Resistant Genes in CPR genomes: 112 For antimicrobial resistance profiling, we carried out an in-house Blast search against the 113 protein databases from ARG-ANNOT (Antibiotic Resistance Gene-ANNOTation)27, BLDB 114 (Beta-Lactamase DataBase)28 and NDARO (National Database of Antibiotic Resistant 115 Organisms)29 containing 2,038, 4,260 and 5,735 sequences, respectively.
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