Abstract
Planococcus is a genus of Gram-positive bacteria known for potential industrial and agricultural applications. Here, we report the first draft genome sequence and phylogenomic analysis of a CRISPR-carrying, multidrug-resistant, novel candidate Planococcus sp. NCCP-2050T isolated from agricultural soil in Pakistan. The strain NCCP-2050T exhibited significant resistance to various classes of antibiotics, including fluoroquinolones (i.e., ciprofloxacin, levofloxacin, ofloxacin, moxifloxacin, and bacitracin), cephalosporins (cefotaxime, ceftazidime, cefoperazone), rifamycins (rifampicin), macrolides (erythromycin), and glycopeptides (vancomycin). Planococcus sp. NCCP-2050T consists of genome size of 3,463,905 bp, comprised of 3639 annotated genes, including 82 carbohydrate-active enzyme genes and 39 secondary metabolite genes. The genome also contained 80 antibiotic resistance, 162 virulence, and 305 pathogen–host interaction genes along with two CRISPR arrays. Based on phylogenomic analysis, digital DNA–DNA hybridization, and average nucleotide identity values (i.e., 35.4 and 88.5%, respectively) it was suggested that strain NCCP-2050T might represent a potential new species within the genus Planococcus.
Abbreviations
- ANI:
-
Average nucleotide identity
- BLAST:
-
Basic local alignment search tool
- CARD:
-
The comprehensive antibiotic resistance database
- CAZy:
-
Carbohydrate-active enzymes
- CGView:
-
Circular genome viewer
- CLSI:
-
Clinical and Laboratory Standards Institute’s guidelines (CLSI, 2020).
- COG:
-
Clusters of Orthologous Groups
- CRISPR:
-
Clustered regularly interspaced short palindromic repeats
- digi-DDH:
-
Digital DNA–DNA hybridization
- GO:
-
Gene ontology
- KEGG:
-
Kyoto Encyclopedia of genes and genomes
- MDR:
-
Multidrug resistant
- MHA:
-
Moller Hinton agar
- NCBI:
-
National Center for Biotechnology Information
- NCCP:
-
National Culture Collection of Pakistan
- PATRIC:
-
Pathosystems Resource Integration Center
- PCR:
-
Polymerase chain reaction
- RAST:
-
Rapid annotations using subsystems technology
- rRNA:
-
Ribosomal ribonucleic acid, ribosomal RNA
- sRNA:
-
Small ribonucleic acid, small RNA
- TMHMM:
-
Transmembrane prediction using Hidden Markov models
- tRNA:
-
Transfer ribonucleic acid
- TSA:
-
Tryptic Soy Agar
- TYGS:
-
Type strain genome server
References
Ahmed I, Yokota A, Fujiwara T (2007) Gracilibacillus boraciitolerans sp. nov., a highly boron-tolerant and moderately halotolerant bacterium isolated from soil. Int J Syst Evol Microbiol 57(4):796–802
Ali A, Liaqat S, Tariq H, Abbas S, Arshad M, Li W-J, Ahmed I (2021a) Neonatal calf diarrhea: a potent reservoir of multi-drug resistant bacteria, environmental contamination and public health hazard in Pakistan. Sci Total Environ 799:149450
Ali A, Tariq H, Abbas S, Arshad M, Li S, Dong L, Li L, Li WJ, Ahmed I (2021b) Draft genome sequence of a multidrug-resistant novel candidate Pseudomonas sp. NCCP-436T isolated from faeces of a bovine host in Pakistan. J Glob Antimicrob Resist 27:91–94. https://doi.org/10.1016/j.jgar.2021.08.011
Arora NK, Mishra I (2023) Responsible consumption and production: a roadmap to sustainable development. Environ Sustain 6:1–6. https://doi.org/10.1007/s42398-023-00266-9
Choi J-H, Im W-T, Liu Q-M, Yoo J-S, Shin J-H, Rhee S-K, Roh D-H (2007) Planococcus donghaensis sp. nov., a starch-degrading bacterium isolated from the East Sea, South Korea. Int J Syst Evol Microbiol 57(11):2645–2650. https://doi.org/10.1099/ijs.0.65036-0
Chokriwal A, Stephen BJ, Jain D, Singh A (2018) Simplistic approach in extracellular synthesis of silver nanoparticles via bioreducing potential of Planococcus plakortidis strain BGCC-51 isolated from dye industry effluent soil. IET Nanobiotechnol 12(5):613–618. https://doi.org/10.1049/iet-nbt.2017.0251
CLSI (2020) Performance Standards for Antimicrobial Susceptibility Testing. 30th ed. CLSI supplement M100. Clinical and Laboratory Standards Institute; Wayne, PA
Engelhardt M, Daly K, Swannell R, Head I (2001) Isolation and characterization of a novel hydrocarbon-degrading, Gram-positive bacterium, isolated from intertidal beach sediment, and description of Planococcus alkanoclasticus sp. nov. J Appl Microbiol 90(2):237–247. https://doi.org/10.1046/j.1365-2672.2001.01241.x
Gao L, Hu J, Zhang X, Wei L, Li S, Miao Z, Chai T (2015) Application of swine manure on agricultural fields contributes to extended-spectrum β-lactamase-producing Escherichia coli spread in Tai’an, China. Front Microbiol 6:313. https://doi.org/10.3389/fmicb.2015.00313
Gopalakrishnan S, Vadlamudi S, Bandikinda P, Sathya A, Vijayabharathi R, Rupela O, Kudapa H, Katta K, Varshney RK (2014) Evaluation of Streptomyces strains isolated from herbal vermicompost for their plant growth-promotion traits in rice. Microbiol Res 169(1):40–48
Gupta RS, Patel S (2020) Robust demarcation of the family Caryophanaceae (Planococcaceae) and its different genera including three novel genera based on phylogenomics and highly specific molecular signatures. Front Microbiol 10:2821
Kim JH, Kang HJ, Yu BJ, Kim SC, Lee PC (2015) Planococcus faecalis sp. nov., a carotenoid-producing species isolated from stools of Antarctic penguins. Int J Syst Evol Microbiol 65(10):3373–3378. https://doi.org/10.1099/ijsem.0.000423
Kour D, Khan SS, Kour H, Kaur T, Devi R, Rai PK, Judy C, McQuestion C, Bianchi A, Spells S (2022) Microbe-mediated bioremediation: current research and future challenges. J Appl Biol Biotechnol 10(2):6–24
Kushwaha K, Saxena J, Agarwal MK (2020) Identification and characterization of psychrotrophic strain of Planococcus maritimus for glucosylated C30 carotenoid production. Indian J Exp Biol 58:190–197. https://doi.org/10.56042/ijeb.v58i03.65442
Li Q, Qiao G, Wang L, Zhang J, Li R, Ni P, Guo Y, Ye S (2019) Studies on bacterial diversity and Vibrio harveyi distribution associated with diseased fugu (Takifugu rubripes) in northeastern China. Pak J Zool 51(1):67–77. https://doi.org/10.17582/journal.pjz/2019.51.1.67.77
Li YX, Wang NN, Zhou YX, Lin CG, Wu JS, Chen XQ, Chen GJ, Du ZJ (2021) Planococcus maritimus ML1206 isolated from wild oysters enhances the survival of Caenorhabditis elegans against Vibrio anguillarum. Mar Drugs. https://doi.org/10.3390/md19030150
Li S, Ondon BS, Ho S-H, Li F (2022) Emerging soil contamination of antibiotics resistance bacteria (ARB) carrying genes (ARGs): new challenges for soil remediation and conservation. Environ Res 219:115132. https://doi.org/10.1016/j.envres.2022.115132
Mališová L, Španělová P, Sedláček I, Pajer P, Musílek M, Puchálková B, Jakubů V, Žemličková H, Šafránková R (2022) The first case of Planococcus glaciei found in blood, a report from the Czech Republic. Folia Microbiol 67(1):121–127
Mann A, Malik S, Rana JS, Nehra K (2021) Whole genome sequencing data of Klebsiella aerogenes isolated from agricultural soil of Haryana, India. Data Brief 38:107311. https://doi.org/10.1016/j.dib.2021.107311
Manyi-Loh C, Mamphweli S, Meyer E, Okoh A (2018) Antibiotic use in agriculture and its consequential resistance in environmental sources: potential public health implications. Molecules 23(4):795. https://doi.org/10.3390/molecules23040795
Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform 14(1):60. https://doi.org/10.1186/1471-2105-14-60
Mykytczuk NC, Wilhelm RC, Whyte LG (2012) Planococcus halocryophilus sp. nov., an extreme sub-zero species from high Arctic permafrost. Int J Syst Evol Microbiol 62(8):1937–1944
Nakagawa Y, Sakane T, Yokota A (1996) Emendation of the Genus Planococcus and Transfer of Flavobacterium okeanokoites Zobell and Upham 1944 to the Genus Planococcus as Planococcus okeanokoites comb. nov. Int J Syst Evol Microbiol 46(4):866–870. https://doi.org/10.1099/00207713-46-4-866
Polianciuc SI, Gurzău AE, Kiss B, Ştefan MG, Loghin F (2020) Antibiotics in the environment: causes and consequences. Med Pharm Rep 93(3):231–240. https://doi.org/10.15386/mpr-1742
Prasanna SN, Venkatesh Kamath B, Pai A, Garge R, Priya MP (2023) Exploring the plethora of hidden potential in the quest for sustainable development: impact of ecological niche on the enzymes from extremophiles. Rasayan J Chem 16(2):573–578. https://doi.org/10.31788/RJC.2023.1628100
Ruangsri J, Kitani Y, Kiron V, Lokesh J, Brinchmann MF, Karlsen BO, Fernandes JM (2013) A novel beta-defensin antimicrobial peptide in Atlantic cod with stimulatory effect on phagocytic activity. PLoS One 8(4):e62302
Styczynski M, Rogowska A, Gieczewska K, Garstka M, Szakiel A, Dziewit L (2020) Genome-based insights into the production of carotenoids by Antarctic bacteria, Planococcus sp. ANT_H30 and Rhodococcus sp. ANT_H53B. Molecules 25(19):4357
Suruttaiyan S, Duraisamy P, Krishnaraj S, Perumalsamy L, Subpiramaniyam S (2022) Isolation, characterization and degradation performance of oxytetracycline degrading bacterium Planococcus sp. strain pw2. Arch Microbiol 204(2):122. https://doi.org/10.1007/s00203-021-02732-6
Walsh F, Duffy B (2013) The culturable soil antibiotic resistome: a community of multi-drug resistant bacteria. PLoS One 8(6):e65567. https://doi.org/10.1371/journal.pone.0065567
Wang Y, Ma L, He J, He Z, Wang M, Liu Z, Li Z, Wang L, Weng S, Guo C (2022) Environmental risk characteristics of bacterial antibiotic resistome in Antarctic krill. Ecotoxicol Environ Saf 232:113289
Yang R, Zhang B, Wang J, Tai X, Sun H, Zhang G, Zhang W, Chen T, Liu G (2020) Planococcus lenghuensis sp. nov., an oil-degrading bacterium isolated from petroleum-contaminated soil. Antonie Van Leeuwenhoek 113(6):839–850. https://doi.org/10.1007/s10482-020-01394-6
Zhang B, Yang R, Zhang G, Liu Y, Zhang D, Zhang W, Chen T, Liu G (2020) Characteristics of Planococcus antioxidans sp. nov., an antioxidant-producing strain isolated from the desert soil in the Qinghai-Tibetan Plateau. Microbiol Open 9(6):1183–1196. https://doi.org/10.1002/mbo3.1028
Funding
This work was supported partly by available resources at NCCP, BCI, and NARC. Additionally, it was also supported in part under Xinjiang Uygur Autonomous Region, Regional Coordinated Innovation Project, and Shanghai Cooperation Organization Science and Technology Partnership Program China (no. 2021E01018). Work was also supported by the Chinese Academy of Sciences President’s International Fellowship Initiative (Grant no. 2020VBA0020).
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IA and AA contributed to conceptualization; AA, SN, YHL, SA, and IA provided methodology; AA, SN, and IA carried out formal analysis; AA, SA, and IA provided software; AA, CM, SA, and IA performed data curation; IA and WJL contributed to project administration, resources, and funding acquisition; IA performed supervision; AA and IA performed writing—original draft; CM, SA, YHL, WJL, and IA performed writing—review and editing.
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Ali, A., Abbas, S., Nawaz, S. et al. Unraveling the draft genome and phylogenomic analysis of a multidrug-resistant Planococcus sp. NCCP-2050T: a promising novel bacteria from Pakistan. 3 Biotech 13, 325 (2023). https://doi.org/10.1007/s13205-023-03748-z
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DOI: https://doi.org/10.1007/s13205-023-03748-z