Skip to main content
SpringerLink
Log in

Characterization of heavy metal-associated bacteria from petroleum-contaminated soil and their resistogram and antibiogram analysis

  • Original Article
  • Published:
Folia Microbiologica Aims and scope Submit manuscript

Abstract

The aim of the current study was to screen and identify heavy metal (chromium, cadmium, and lead) associated bacteria from petroleum-contaminated soil of district Muzaffarabad, Azad Jammu and Kashmir, Pakistan to develop ecofriendly technology for contaminated soil remediation. The petroleum-contaminated soil was collected from 99 different localities of district Muzaffarabad and the detection of heavy metals via an atomic absorption spectrometer. The isolation and identification of heavy metals-associated bacteria were done via traditional and molecular methods. Resistogram and antibiogram analysis were also performed using agar well diffusion and agar disc diffusion methods. The isolated bacteria were classified into species, i.e., B. paramycoides, B. albus, B. thuringiensis, B. velezensis, B. anthracis, B. pacificus Burkholderia arboris, Burkholderia reimsis, Burkholderia aenigmatica, and Streptococcus agalactiae. All heavy metals-associated bacteria showed resistance against both high and low concentrations of chromium while sensitive towards high and low concentrations of lead in the range of 3.0 ± 0.0 mm to 13.0 ± 0.0 mm and maximum inhibition was recorded when cadmium was used. Results revealed that some bacteria showed sensitivity towards Sulphonamides, Norfloxacin, Erythromycin, and Tobramycin. It was concluded that chromium-resistant bacteria could be used as a favorable source for chromium remediation from contaminated areas and could be used as a potential microbial filter.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Availability of data and materials

Most of the data generated during this study are included in this article. However, raw data sheets are available from the corresponding as well as co-authors upon reasonable request.

References

  • Abioye OP, Oyewole OA, Oyeleke SB, Adeyemi MO, Orukotan AA (2018) Biosorption of lead, chromium and cadmium in tannery effluent using indigenous microorganisms. Braz J Biol Sci 5(9):25–32

    Article  Google Scholar 

  • Abo-Amer AE, Abu-Gharbia MA, Soltan ESM, Abd El-Raheem WM (2014) Isolation and molecular characterization of heavy metal-resistant Azotobacter chroococcum from agricultural soil and their potential application in bioremediation. Geomicrobiol J 31(7):551–561

    Article  CAS  Google Scholar 

  • Achal V, Kumari D, Pan X (2011) Bioremediation of chromium contaminated soil by abrown-rot fungus. Gloeophyllum Sepiarium Res J Microbiol 6(2):166

    CAS  Google Scholar 

  • Ahemad M, Malik A (2011) Bioaccumulation of heavy metals by zinc resistant bacteria isolated from agricultural soils irrigated with wastewater. Bacteriol J 2(1):12–21

    Article  Google Scholar 

  • Aka NRJ, Babalola OO (2017) Identification and characterization of Cr-, Cd-, and Ni-tolerant bacteria isolated from mine tailings. Bioremediat J 21(1):1–19

    Article  CAS  Google Scholar 

  • Ashokkumar P, Loashini VM, Bhavya V (2017) Effect of pH, temperature and biomass on biosorption of heavy metals by Sphaerotilus natans. Int j Microbiol Mycol 6(1):32–38

    Google Scholar 

  • Ashruta GA, Nanoty V, Bhalekar U (2014) Biosorption of heavy metals from aqueous solution using bacterial EPS. Int J Life Sci 2:373–377

    Google Scholar 

  • Bauer AW, Perry DM, Kirby WM (1959) Single-disk antibiotic-sensitivity testing of staphylococci: an analysis of technique and results. Arc Internal Med 104(2):208–216

    CAS  Google Scholar 

  • Bilgin M, Tulun S (2016) Removal of heavy metals (Cu, Cd and Zn) from contaminated soils using EDTA and FeCl3. Glob Nest J 18:98–107

    Article  CAS  Google Scholar 

  • Brown DF, Kothari D (1975) Comparison of antibiotic discs from different sources. J Clini Pathol 28(10):779–783

    Article  CAS  Google Scholar 

  • Chandrasekaran A, Ravisankar R, Harikrishnan N, Satapathy KK, Prasad MVR, Kanagasabapathy KV (2015) Multivariate statistical analysis of heavy metal concentration in soils of Yelagiri Hills, Tamilnadu, India-Spectroscopical 59 approach. Spectrochim Acta A Mol Biomol 137:589–600

    Article  ADS  CAS  Google Scholar 

  • Chang JS, Kim YH, Kim KW (2008) The ars genotype characterization of arsenic resistant bacteria from arsenic-contaminated gold–silver mines in the Republic of Korea. Appl Microbiol Biotechnol APPL 80(1):155–165

    Article  CAS  Google Scholar 

  • Chatterjee S, Chatterjee NC, Dutta S (2012) Bioreduction of chromium (VI) to chromium (III) by a novel yeast strain Rhodotorula mucilaginosa (MTCC 9315). Afr J Biotechnol 11(83):14920–14929

    CAS  Google Scholar 

  • Chen LC, Zhu Y, Papandreou G, Schroff F, Adam H (2018) Encoder-decoder with atrous separable convolution for semantic image segmentation. In Proceedings of the European conference on computer vision (ECCV) pp 801–818

  • Chinedu E, Chukwuemeka CK (2018) Oil spillage and heavy metals toxicity risk in the Niger Delta. Nigeria J Health Pollut 8(19):180905

    Article  PubMed  Google Scholar 

  • De J, Ramaiah N, Vardanyan L (2008) Detoxification of toxic heavy metals by marine bacteria highly resistant to mercury. Mar Biotechnol 10(4):471–477

    Article  CAS  Google Scholar 

  • de la Cueva SC, Rodríguez CH, Cruz NOS, Contreras JAR, Miranda JL (2016) Changes in bacterial populations during bioremediation of soil contaminated with petroleum hydrocarbons. Water Air Soil Pollut 227:1–12

    Google Scholar 

  • Di Cesare A, Eckert EM, D’Urso S, Bertoni R, Gillan DC, Wattiez R, Corno G (2016) Co-occurrence of integrase 1, antibiotic and heavy metal resistance genes in municipal wastewater treatment plants. Water Res 94:208–214

    Article  PubMed  Google Scholar 

  • Dixit R, Wasiullah MD, Pandiyan K, Singh UB, Sahu A, Shukla R, Singh BP, Rai JP, Sharma PK et al (2015) Bioremediation of heavy metals from soil and aquatic environment: an overview of principles and criteria of fundamental processes. Sustainability 7(2):2189–2212

    Article  Google Scholar 

  • Duruibe JO, Ogwuegbu MOC, Egwurugwu JN (2007) Heavy metal pollution and human biotoxic effects. IJPS 2(5):112–118

    Google Scholar 

  • Ekperusi OA, Aigbodion IF (2015) Bioremediation of heavy metals and petroleum hydrocarbons in diesel contaminated soil with the earthworm. Springerplus 4(1):1–13

    Article  CAS  Google Scholar 

  • Galal TM, Gharib FA, Ghazi SM, Mansour KH (2017) Phytostabilization of heavy metals by the emergent macrophyte Vossia cuspidata (Roxb.) Griff.: a 61 phytoremediation approach. Int J Phytoremediation 19(11):992999

  • Gautam RK, Mudhoo A, Lofrano G, Chattopadhyaya MC (2014) Biomass-derived biosorbents for metal ions sequestration: adsorbent modification and activation methods and adsorbent regeneration. J Environ Chem Eng 2(1):239–259

    Article  CAS  Google Scholar 

  • Guerra AM, Aimedieu P, Bornert M, Cui YJ, Tang AM, Sun Z, Bernier F (2018) Analysis of the structural changes of a pellet/powder bentonite mixture upon wetting by X-ray computed microtomography. Appl Clay Sci 165:164–169

    Article  Google Scholar 

  • Hammer KA, Carson CF, Riley TV (1999) Antimicrobial activity of essential oils and other plant extracts. J Appl Microbiol 86(6):985–990

    Article  CAS  PubMed  Google Scholar 

  • Hu HW, Wang JT, Li J, Li JJ, Ma YB, Chen D, He JZ (2016) Field-based evidence for copper contamination induced changes of antibiotic resistance in agricultural soils. Environ Microbiol 18(11):3896–3909

    Article  CAS  PubMed  Google Scholar 

  • Huan L, Haixia Z, Longhua W, Anna L, Fang-Jie Z, Wenzhong X (2017) Heavy metal ATPase 3 (HMA3) confers cadmium hypertolerance on the cadmium/zinc hyperaccumulator Sedum plumbizincicola. New Phytol 15:687–698

    Google Scholar 

  • Huang D, Hu C, Zeng G, Cheng M, Xu P, Gong X, Wang R, Xue W (2016) Combination of Fenton processes and biotreatment for wastewater treatment and soil remediation. Sci Total Environ 574:1599–1610

    Article  ADS  PubMed  Google Scholar 

  • Huerta B, Marti E, Gros M, López P, Pompêo M, Armengol J, Marcé R (2013) Exploring the links between antibiotic occurrence, antibiotic resistance, and bacterial communities in water supply reservoirs. Sci Total Environ 456:161–170

    Article  ADS  PubMed  Google Scholar 

  • Idodo-Umeh G, Ogbeibu AE (2010) Bioaccumulation of the heavy metals in cassava tubers and plantain fruits grown in soils impacted with petroleum and non-petroleum activities. Res J Environ Sci 4(1):33–41

    Article  CAS  Google Scholar 

  • Igiri BE, Okoduwa SI, Idoko GO, Akabuogu EP, Adeyi AO, Ejiogu IK (2018) Toxicity and bioremediation of heavy metals contaminated ecosystem from tannery wastewater: a review. J Toxicol 2018

  • Jafari SA, Cheraghi S, Mirbakhsh M, Mirza R, Maryamabadi A (2015) Employing response surface methodology for optimization of mercury bioremediation by Vibrio parahaemolyticus PG02 in coastal sediments of Bushehr Iran. CLEAN–Soil Air Water 43(1):118–126

  • Jayakumar K, Rajesh M, Baskaran L, Vijayarengan P (2013) Changes in nutritional metabolism of tomato (Lycopersicon esculantum Mill.) plants exposed to increasing concentration of cobalt chloride. Int J Food Sci Nutr 4(2):62–69

  • Jinadasa N, Collins D, Holford P, Milham PJ, Conroy JP (2016) Reactions to cadmium stress in a cadmium-tolerant variety of cabbage (Brassica oleracea L.): is cadmium tolerance necessarily desirable in food crops. ESPR 23(6):5296–5306

  • Karakagh RM, Chorom M, Motamedi H, Kalkhajeh YK, Oustan S (2012) Biosorption of Cd and Ni by inactivated bacteria isolated from agricultural soil treated with sewage sludge. Ecohydrol Hydrobiol 12(3):191–198

    Article  CAS  Google Scholar 

  • Khusro A, Preetam Raj JP, Panicker SG (2014) Multiple heavy metals response and antibiotic sensitivity pattern of Bacillus subtilis strain KPA. J Chem Pharm Res 6:532–538

    CAS  Google Scholar 

  • Kim HS, Kim YJ, Seo YR (2015a) An overview of carcinogenic heavy metal: molecular toxicity mechanism and prevention. J Cancer Prev 20(4):232

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim IH, Choi JH, Joo JO, Kim YK, Choi JW, Oh BK (2015b) Development of a microbe-zeolite carrier for the effective elimination of heavy metals from seawater. J Microbiol Biotechnol 25(9):1542–1546

    Article  CAS  PubMed  Google Scholar 

  • Ksheminska H, Fedorovych D, Honchar T, Ivash M, Gonchar M (2008) Yeast tolerance to chromium depends on extracellular chromate reduction and Cr (III) chelation. Food Technol Biotechnol 46(4):419–426

    CAS  Google Scholar 

  • Kumar R, Bhatia D, Singh R, Rani S, Bishnoi NR (2011) Sorption of heavy metals from electroplating effluent using immobilized biomass Trichoderma viride in a continuous packed-bed column. Int Biodeterior Biodegradation 65(8):1133–1139

    Article  CAS  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X. Molecular Evolutionary Genetics Analysis across Computing Platforms Mol Bio Evo 35:1547–1549

    CAS  Google Scholar 

  • Kumaran NS, Sundaramanicam A, Bragadeeswaran S (2011) Adsorption studies on heavy metals by isolated cyanobacterial strain (nostoc sp.) from uppanar estuarine water, southeast coast of India. J Appl Sci 7(11):16091615

  • Lakkireddy K, Kües U (2017) Bulk isolation of basidiospores from wild mushrooms by electrostatic attraction with low risk of microbial contaminations. AMB Express 7(1):1–22

    Article  Google Scholar 

  • Li P, Li J, Feng X, Li J, Hao Y, Zhang J, Wang B (2019) Metal-organic frameworks with photocatalytic bactericidal activity for integrated air cleaning. Nat Commun 10:1–10

    ADS  Google Scholar 

  • Lianwen L, Wei L, Weiping S, Mingxin G (2018) Remediation techniques for heavy metal-contaminated soils: principles and applicability. Sci Total Environ 633:206–219

    Article  ADS  Google Scholar 

  • Luna JM, Rufino RD, Sarubbo LA (2016) Biosurfactant from Candida sphaerica UCP0995 exhibiting heavy metal remediation properties. Process Saf Environ Prot 102:558–566

    Article  CAS  Google Scholar 

  • Ma L, Wang Q, Islam SM, Liu Y, Ma S, Kanatzidis MG (2016) Highly selective and efficient removal of heavy metals by layered double hydroxide intercalated with the MoS42–ion. J Amer Chem Soci 138:2858–2866

    Article  CAS  Google Scholar 

  • Manivasagaperumal R, Balamurugan S, Thiyagarajan G, Sekar J (2011) Effect of zinc on germination, seedling growth and biochemical content of cluster bean (Cyamopsis tetragonoloba (L.) Taub). Curr Plant Biol 2(5):11–15

  • Martínez Álvarez LM, Lo Balbo A, Mac Cormack WP, Ruberto LAM (2015) Bioremediation of a petroleum hydrocarbon-contaminated Antarctic soil: optimization of a biostimulation strategy using response-surface methodology (RSM). Cold Reg Sci Technol 119:61–67

    Article  Google Scholar 

  • Mosa KA, Saadoun I, Kumar K, Helmy M, Dhankher OP (2016) Potential biotechnological strategies for the cleanup of heavy metals and metalloids. Front Plant Sci 7:303

    Article  PubMed  PubMed Central  Google Scholar 

  • Muhlbachova G, Sagova-Mareckova M, Omelka M, Szakova J, Tlustos P (2015) The influence of soil organic carbon on interactions between microbial parameters and metal concentrations at a long-term contaminated site. Sci Total Environ 502:218–223

    Article  ADS  CAS  PubMed  Google Scholar 

  • Naseer A, Andleeb S, Basit A, Abbasi WA, Ejaz S, Ali S, Ali NM (2022) Phylogenetic illustration of Eisenia fetida associated vermi-bacteria involved in heavy metals remediation and retaining plant growth promoting traits. J Oleo Sci 71(8):1241–1252

    Article  CAS  PubMed  Google Scholar 

  • Okolo NV, Olowolafe EA, Akawu I, Okoduwa SIR (2016) Effects of industrial effluents on soil resources in Challawa industrial area. Kano, Nigeria Glob Ecol Conserv 5(1):1–10

    Google Scholar 

  • Pacwa-Płociniczak M, Płaza GA, Poliwoda A, Piotrowska-Seget Z (2014) Characterization of hydrocarbon-degrading and biosurfactant-producing Pseudomonas sp. P-1 strain as a potential tool for bioremediation of petroleum-contaminated soil. Environ Sci Pollut Res 21(15):9385–9395

  • Parvathi K, Nagendran R, Nareshkumar R (2007) Effect of pH on chromium biosorption by chemically treated Saccharomyces.

  • Puyen ZM, Villagrasa E, Maldonado J, Diestra E, Esteve I, Solé A (2012) Biosorption of lead and copper by heavy-metal tolerant Micrococcus luteus DE2008. Bioresour Technol 126:233–237

    Article  CAS  PubMed  Google Scholar 

  • Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28(3):142–149

    Article  CAS  PubMed  Google Scholar 

  • Rehman A, Anjum MS (2011) Multiple metal tolerance and biosorption of cadmium by Candida tropicalis isolated from industrial effluents: glutathione as detoxifying agent. Environ Monit Assess 174(1):585–595

    Article  CAS  PubMed  Google Scholar 

  • Rezania S, Taib SM, Din MFM, Dahalan FA, Kamyab H (2016) Comprehensive review on phytotechnology: heavy metals removal by diverse aquatic plants species from wastewater. J Hazard Mater 318:587–599

    Article  CAS  PubMed  Google Scholar 

  • Rios JL, Recio MC, Villar A (1988) Screening methods for natural products with antimicrobial activity: a review of the literature. J Ethnopharmacol 23(2–3):127–149

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Mozaz S, Chamorro S, Marti E, Huerta B, Gros M, Sànchez-Melsió A, Balcázar JL (2015) Occurrence of antibiotics and antibiotic resistance genes in hospital and urban wastewaters and their impact on the receiving river. Water Res 69:234–242

    Article  CAS  PubMed  Google Scholar 

  • Sarah GH, Thaura GH (2021) Heavy metals in soils and the remediation potential of bacteria associated with the plant microbiome. Frontiers Environ Sci 9:604216

    Article  Google Scholar 

  • Seeley HW, Vandemark PJ, Lee JJ (2001) Microbes in action: a laboratory manual of microbiology, W.H. Freeman and Company, New York, NY, USA, 4th edition

  • Siddiquee S, Rovina K, Azad SA, Naher L, Suryani S, Chaikaew P (2015) Heavy metal contaminants removal from wastewater using the potential filamentous fungi biomass: a review. J Microb Biochem Technol 7(6):384–395

    Article  CAS  Google Scholar 

  • Singh N, Verma T, Gaur R (2013) Detoxification of hexavalent chromium by an indigenous facultative anaerobic Bacillus cereus strain isolated from tannery effluent. Afr J Biotechnol 12(10)

  • Smith E, Thavamani P, Ramadass K, Naidu R, Srivastava P, Megharaj M (2015) Remediation trials for hydrocarbon-contaminated soils in arid environments: evaluation of bioslurry and biopiling techniques. Int Biodeterior Biodegradation 101:56–65

    Article  CAS  Google Scholar 

  • Somasegaran P, Hoben HJ (1994) Quantifying the growth of rhizobia. Handbook for Rhizobia Springer New York NY 47–57

  • Srivastava S, Agrawal SB, Mondal MK (2015) A review on progress of heavy metal removal using adsorbents of microbial and plant origin. Environ Sci Pollut Res 22(20):15386–15415

    Article  Google Scholar 

  • Su C (2014) A review on heavy metal contamination in the soil worldwide: situation, impact and remediation techniques. Environ Skep Crit 3:24–38

    Google Scholar 

  • Sumiahadi A, Acar R (2018) A review of phytoremediation technology: heavy metals uptake by plants. Earth Env Sci 142:12–23

    Google Scholar 

  • Sun Y (2009) On-site management of International Petroleum Cooperation Projects. Natural Gas Exploration and Development 32(2):69–73

    Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the Number of Nucleotide Substitutions in the Control Region of Mitochondrial DNA in Humans and Chimpanzees Mol Bio Evo 10:512–526

    CAS  Google Scholar 

  • Taştan BE, Ertuğrul S, Dönmez G (2010) Effective bioremoval of reactive dye and heavy metals by Aspergillus versicolor. Bioresour Technol 101(3):870–876

    Article  PubMed  Google Scholar 

  • Tremblay MS, Aubert S, Barnes JD, Saunders TJ, Carson V, Latimer-Cheung AE, Chinapaw MJ (2017) Sedentary behavior research network (SBRN)–terminology consensus project process and outcome. IJBNPA 14(1):1–17

    Google Scholar 

  • Verma S, Kuila A (2019) Bioremediation of heavy metals by microbial process. Environ Technol Innov 14:100369

    Article  Google Scholar 

  • Wakelin S, Gerard E, Black A, Hamonts K, Condron L, Yuan T, O’Callaghan M (2014) Mechanisms of pollution induced community tolerance in a soil microbial community exposed to Cu. Environ Pollut 190:1–9

    Article  CAS  PubMed  Google Scholar 

  • Wan J, Zhang C, Zeng G, Huang D, Hu L, Huang C, Wang L (2016) Synthesis and evaluation of a new class of stabilized nano-chlorapatite for Pb immobilization in sediment. J Hazard Mater 320:278–288

    Article  CAS  PubMed  Google Scholar 

  • Yang T, Chen M, Wang J (2015) Genetic and chemical modification of cells for selective separation and analysis of heavy metals of biological or environmental significance. TrAC, Trends Anal Chem 66:90–102

    Article  CAS  Google Scholar 

  • Zheng X, Chen L, Chen M, Chen J, Li X (2019) Functional metagenomics to mine soil microbiome for novel cadmium resistance genetic determinants. Pedosphere 29(3):298–310

    Article  CAS  Google Scholar 

  • Zhu S, Meng Q, Wang L, Zhang J, Song Y, Jin H, Yang B (2013) Highly photoluminescent carbon dots for multicolor patterning, sensors, and bioimaging. Angew Chem 125(14):4045–4049

    Article  ADS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Microbial Biotechnology and Vermi-Technology Laboratory, Department of Zoology, The University of Azad Jammu & Kashmir, King Abdullah Campus, Chattar Kalass, Muzaffarabad, 13100, Pakistan

    Abdul Basit, Saiqa Andleeb, Nasra Ashraf, Anum Naseer & Fahad Kiyani

  2. Department of Zoology, GC University, Lahore, Pakistan

    Iram Liaqat & Shaukat Ali

  3. Institute of Botany, University of the Punjab, Quaid-E-Azam Campus, Lahore, Pakistan

    Aisha Nazir

Authors
  1. Abdul Basit
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Saiqa Andleeb
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Iram Liaqat
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nasra Ashraf
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shaukat Ali
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Anum Naseer
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Aisha Nazir
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Fahad Kiyani
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Saiqa Andleeb conceived the idea, designed the experiments, analyzed and interpreted the results, and was a major contributor to manuscript writing. Abdul Basit, Fahad Kiyani, and Anum Naseer performed all the experiments and wrote the first draft of the manuscript. Iram Liaqat helped in bioinformatics tools for phylogenetic data analysis. Shaukat Ali, Aisha Nazir, and Nasra Ashraf contributed to formal analysis, interpreted results, and manuscript review.

Corresponding author

Correspondence to Saiqa Andleeb.

Ethics declarations

Consent for publication

Not applicable.

Consent to participate

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Basit, A., Andleeb, S., Liaqat, I. et al. Characterization of heavy metal-associated bacteria from petroleum-contaminated soil and their resistogram and antibiogram analysis. Folia Microbiol (2024). https://doi.org/10.1007/s12223-024-01135-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12223-024-01135-6

Keywords

Search

Navigation