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Identification and in-depth characterization of clinical isolates of Peribacillus frigoritolerans.

Λεπτομέρειες βιβλιογραφικής εγγραφής
Τίτλος: Identification and in-depth characterization of clinical isolates of Peribacillus frigoritolerans.
Συγγραφείς: Calvigioni M; Department of Translational Research and New Technologies in Medicine and Surgery, University of Pisa, Pisa, Italy., Rossi V; Department of Translational Research and New Technologies in Medicine and Surgery, University of Pisa, Pisa, Italy., Celandroni F; Department of Translational Research and New Technologies in Medicine and Surgery, University of Pisa, Pisa, Italy., Barnini S; Azienda Ospedaliero-Universitaria Pisana, Pisa, Italy., Lupetti A; Department of Translational Research and New Technologies in Medicine and Surgery, University of Pisa, Pisa, Italy.; Azienda Ospedaliero-Universitaria Pisana, Pisa, Italy., Mazzantini D; Department of Translational Research and New Technologies in Medicine and Surgery, University of Pisa, Pisa, Italy., Ghelardi E; Department of Translational Research and New Technologies in Medicine and Surgery, University of Pisa, Pisa, Italy.; Azienda Ospedaliero-Universitaria Pisana, Pisa, Italy.
Πηγή: Microbiology spectrum [Microbiol Spectr] 2026 Aug 04; Vol. 14 (8), pp. e0024526. Date of Electronic Publication: 2026 Jul 15.
Τύπος έκδοσης: Journal Article
Γλώσσα: English
Στοιχεία περιοδικού: Publisher: ASM Press Country of Publication: United States NLM ID: 101634614 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 2165-0497 (Electronic) Linking ISSN: 21650497 NLM ISO Abbreviation: Microbiol Spectr Subsets: MEDLINE
Imprint Name(s): Original Publication: Washington, DC : ASM Press, 2013-
Ιατρικοί όροι (MeSH): Bacillaceae*/genetics , Bacillaceae*/isolation & purification , Bacillaceae*/classification , Bacillaceae*/drug effects , Gram-Positive Bacterial Infections*/microbiology, RNA, Ribosomal, 16S/genetics ; Anti-Bacterial Agents/pharmacology ; Virulence Factors/genetics ; Biofilms/growth & development ; Humans ; Whole Genome Sequencing ; Virulence ; Phylogeny ; Microbial Sensitivity Tests ; Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization ; Drug Resistance, Bacterial ; Genome, Bacterial
Περίληψη: Peribacillus frigoritolerans is a bacterial species commonly found in the environment and used as a plant-growth promoter and biocontrol agent in agriculture. Recent evidence has proven that Peribacillus spp. are also able to cause severe infections in humans, thus emerging as new human pathogens. In this study, for the first time, 10 P. frigoritolerans strains were isolated from human samples (both superficial and sterile deep body sites) and characterized in terms of morphology, lifestyle, genetics, and virulence. The molecular identification by MALDI-TOF mass spectrometry and 16S rRNA gene sequencing was inconclusive, while whole-genome sequencing was effective in properly identifying isolates within the species P. frigoritolerans. The pangenome analysis provided an overview of the virulence potential of P. frigoritolerans, revealing the presence of genes involved in antibiotic resistance and toxin/exoenzyme production. Phenotypically, the strains displayed different features and behaviors, indicating strain-specific properties and high intra-species variability. A part of the strains exhibited virulence factors, being able to swim and swarm, form biofilms, and produce enzymes and toxins. Antibiotic susceptibility testing revealed resistance to ampicillin for all strains and resistance to erythromycin and clindamycin for some of them. Antimicrobial activity against Gram-positive bacteria and fungi was demonstrated, further corroborating the presence of putative bacteriocin/antimicrobial peptide-encoding genes. An association between the overall virulence potential and infection site/severity was hypothesized. Altogether, these findings highlight the extreme diversity within the species, reveal the strain-dependent pathogenic potential of P. frigoritolerans, and support its role as a candidate human pathogen.
Importance: This study provides insights into the infectious role of Peribacillus frigoritolerans, an almost unknown bacterial species with agrobiotechnological potential but no history of human infections. This is the first report of P. frigoritolerans isolation from human clinical samples. Ten P. frigorit-olerans strains were herein characterized for their morphology, lifestyle, genetics, and virulence, highlighting an extreme intra-species variability and the potential to act as pathogens in humans. Importantly, this study points out the need for unconventional methods for proper identification of this species, since traditional techniques result inconclusive. Resistance to commonly prescribed antibiotics was also evidenced, confirming the importance of antimicrobial testing on clinical iso-lates. This study lays the foundation for a more in-depth characterization of Peribacillus spp. in the clinical context.
Competing Interests: The authors declare no conflict of interest.
References: Sci Total Environ. 2023 Apr 15;869:161809. (PMID: 36702282)
Nucleic Acids Res. 2023 Jan 6;51(D1):D690-D699. (PMID: 36263822)
Curr Microbiol. 2020 Aug;77(8):1916-1923. (PMID: 32248281)
Microb Genom. 2021 Nov;7(11):. (PMID: 34739369)
J Appl Microbiol. 2022 Aug;133(2):1078-1088. (PMID: 35611609)
Int J Biol Macromol. 2024 Oct;277(Pt 4):134583. (PMID: 39122074)
Pest Manag Sci. 2024 Feb;80(2):724-733. (PMID: 37774135)
Nat Commun. 2020 May 19;11(1):2500. (PMID: 32427907)
Front Microbiol. 2018 Aug 17;9:1946. (PMID: 30174669)
Nat Commun. 2019 May 16;10(1):2182. (PMID: 31097708)
Biocontrol Sci. 2021;26(2):67-74. (PMID: 34092716)
Curr Microbiol. 2023 Jan 20;80(2):80. (PMID: 36662359)
J Appl Microbiol. 2024 Apr 1;135(4):. (PMID: 38486365)
Biotechnol J. 2024 Jan;19(1):e2300330. (PMID: 38180313)
Int J Syst Evol Microbiol. 2020 Jan;70(1):406-438. (PMID: 31617837)
Front Microbiol. 2024 Jul 03;15:1415400. (PMID: 39021634)
Bioinformatics. 2015 Nov 15;31(22):3691-3. (PMID: 26198102)
ACS Omega. 2023 Sep 13;8(38):34982-34994. (PMID: 37779958)
Microb Pathog. 2021 Jan;150:104734. (PMID: 33429050)
Emerg Microbes Infect. 2022 Dec;11(1):2340-2349. (PMID: 36032037)
Front Plant Sci. 2025 Apr 15;16:1570986. (PMID: 40303853)
Bioinformatics. 2014 May 1;30(9):1312-3. (PMID: 24451623)
Gene. 2024 Jul 1;914:148395. (PMID: 38531176)
J Bacteriol. 1991 Jan;173(2):697-703. (PMID: 1987160)
Microorganisms. 2023 Oct 12;11(10):. (PMID: 37894197)
Microorganisms. 2022 Nov 28;10(12):. (PMID: 36557608)
Methods Mol Biol. 2020;2075:285-294. (PMID: 31584170)
Environ Microbiol Rep. 2024 Dec;16(6):e70053. (PMID: 39604090)
Front Microbiol. 2023 Sep 01;14:1219581. (PMID: 37720141)
Int J Food Microbiol. 2015 Mar 16;197:30-9. (PMID: 25555227)
Microbiol Spectr. 2019 Nov;7(6):. (PMID: 31858953)
Nat Biotechnol. 2023 Nov;41(11):1633-1644. (PMID: 36823356)
Nucleic Acids Res. 2022 Jan 7;50(D1):D912-D917. (PMID: 34850947)
Pathogens. 2022 Oct 18;11(10):. (PMID: 36297260)
Access Microbiol. 2025 Jan 14;7(1):. (PMID: 39810798)
Microorganisms. 2023 Sep 05;11(9):. (PMID: 37764079)
Microbiol Resour Announc. 2022 May 19;11(5):e0015222. (PMID: 35389269)
J Comput Biol. 2012 May;19(5):455-77. (PMID: 22506599)
Sci Rep. 2022 Nov 7;12(1):18883. (PMID: 36344604)
J Hazard Mater. 2024 Jan 5;461:132539. (PMID: 37717445)
Proc Natl Acad Sci U S A. 1965 Sep;54(3):704-11. (PMID: 4956288)
Nucleic Acids Res. 2018 Jul 2;46(W1):W278-W281. (PMID: 29788290)
J Bacteriol. 2023 Jun 27;205(6):e0013323. (PMID: 37195186)
Front Microbiol. 2023 Dec 08;14:1290697. (PMID: 38143858)
Front Microbiol. 2023 May 05;14:1127321. (PMID: 37234535)
Arch Microbiol. 2022 Feb 4;204(3):162. (PMID: 35119529)
Clin Infect Dis. 2007 Jan 15;44(2):280-6. (PMID: 17173232)
Environ Microbiol. 2012 Nov;14(11):2870-90. (PMID: 22882546)
Saudi J Biol Sci. 2020 Oct;27(10):2660-2668. (PMID: 32994725)
Sci Rep. 2024 Oct 22;14(1):24909. (PMID: 39438497)
Appl Environ Microbiol. 2022 Sep 27;88(18):e0099122. (PMID: 36036594)
Curr Microbiol. 2020 Oct;77(10):2896-2903. (PMID: 32651608)
Contributed Indexing: Keywords: Peribacillus frigoritolerans; antibiotic resistance; genome analysis; identification; microbiological characterization; virulence potential
Substance Nomenclature: 0 (RNA, Ribosomal, 16S)
0 (Anti-Bacterial Agents)
0 (Virulence Factors)
Entry Date(s): Date Created: 20260715 Date Completed: 20260807 Latest Revision: 20260923
Update Code: 20260923
PubMed Central ID: PMC13436373
DOI: 10.1128/spectrum.00245-26
PMID: 42454910
Βάση Δεδομένων: MEDLINE
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  Data: Identification and in-depth characterization of clinical isolates of Peribacillus frigoritolerans.
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  Data: <searchLink fieldCode="AU" term="%22Calvigioni+M%22">Calvigioni M</searchLink>; Department of Translational Research and New Technologies in Medicine and Surgery, University of Pisa, Pisa, Italy.<br /><searchLink fieldCode="AU" term="%22Rossi+V%22">Rossi V</searchLink>; Department of Translational Research and New Technologies in Medicine and Surgery, University of Pisa, Pisa, Italy.<br /><searchLink fieldCode="AU" term="%22Celandroni+F%22">Celandroni F</searchLink>; Department of Translational Research and New Technologies in Medicine and Surgery, University of Pisa, Pisa, Italy.<br /><searchLink fieldCode="AU" term="%22Barnini+S%22">Barnini S</searchLink>; Azienda Ospedaliero-Universitaria Pisana, Pisa, Italy.<br /><searchLink fieldCode="AU" term="%22Lupetti+A%22">Lupetti A</searchLink>; Department of Translational Research and New Technologies in Medicine and Surgery, University of Pisa, Pisa, Italy.; Azienda Ospedaliero-Universitaria Pisana, Pisa, Italy.<br /><searchLink fieldCode="AU" term="%22Mazzantini+D%22">Mazzantini D</searchLink>; Department of Translational Research and New Technologies in Medicine and Surgery, University of Pisa, Pisa, Italy.<br /><searchLink fieldCode="AU" term="%22Ghelardi+E%22">Ghelardi E</searchLink>; Department of Translational Research and New Technologies in Medicine and Surgery, University of Pisa, Pisa, Italy.; Azienda Ospedaliero-Universitaria Pisana, Pisa, Italy.
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  Data: <searchLink fieldCode="JN" term="%22101634614%22">Microbiology spectrum</searchLink> [Microbiol Spectr] 2026 Aug 04; Vol. 14 (8), pp. e0024526. <i>Date of Electronic Publication: </i>2026 Jul 15.
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  Data: <i>Publisher: </i><searchLink fieldCode="PB" term="%22ASM+Press%22">ASM Press </searchLink><i>Country of Publication: </i>United States <i>NLM ID: </i>101634614 <i>Publication Model: </i>Print-Electronic <i>Cited Medium: </i>Internet <i>ISSN: </i>2165-0497 (Electronic) <i>Linking ISSN: </i><searchLink fieldCode="IS" term="%2221650497%22">21650497 </searchLink><i>NLM ISO Abbreviation: </i>Microbiol Spectr <i>Subsets: </i>MEDLINE
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  Data: <i>Original Publication</i>: Washington, DC : ASM Press, 2013-
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  Data: <searchLink fieldCode="MM" term="%22Bacillaceae%22">Bacillaceae*</searchLink>/<searchLink fieldCode="MM" term="%22Bacillaceae+genetics%22">genetics</searchLink> <br /><searchLink fieldCode="MM" term="%22Bacillaceae%22">Bacillaceae*</searchLink>/<searchLink fieldCode="MM" term="%22Bacillaceae+isolation+%26+purification%22">isolation & purification</searchLink> <br /><searchLink fieldCode="MM" term="%22Bacillaceae%22">Bacillaceae*</searchLink>/<searchLink fieldCode="MM" term="%22Bacillaceae+classification%22">classification</searchLink> <br /><searchLink fieldCode="MM" term="%22Bacillaceae%22">Bacillaceae*</searchLink>/<searchLink fieldCode="MM" term="%22Bacillaceae+drug+effects%22">drug effects</searchLink> <br /><searchLink fieldCode="MM" term="%22Gram-Positive+Bacterial+Infections%22">Gram-Positive Bacterial Infections*</searchLink>/<searchLink fieldCode="MM" term="%22Gram-Positive+Bacterial+Infections+microbiology%22">microbiology</searchLink><br /><searchLink fieldCode="MH" term="%22RNA%2C+Ribosomal%2C+16S%22">RNA, Ribosomal, 16S</searchLink>/<searchLink fieldCode="MH" term="%22RNA%2C+Ribosomal%2C+16S+genetics%22">genetics</searchLink> ; <searchLink fieldCode="MH" term="%22Anti-Bacterial+Agents%22">Anti-Bacterial Agents</searchLink>/<searchLink fieldCode="MH" term="%22Anti-Bacterial+Agents+pharmacology%22">pharmacology</searchLink> ; <searchLink fieldCode="MH" term="%22Virulence+Factors%22">Virulence Factors</searchLink>/<searchLink fieldCode="MH" term="%22Virulence+Factors+genetics%22">genetics</searchLink> ; <searchLink fieldCode="MH" term="%22Biofilms%22">Biofilms</searchLink>/<searchLink fieldCode="MH" term="%22Biofilms+growth+%26+development%22">growth & development</searchLink> ; <searchLink fieldCode="MH" term="%22Humans%22">Humans</searchLink> ; <searchLink fieldCode="MH" term="%22Whole+Genome+Sequencing%22">Whole Genome Sequencing</searchLink> ; <searchLink fieldCode="MH" term="%22Virulence%22">Virulence</searchLink> ; <searchLink fieldCode="MH" term="%22Phylogeny%22">Phylogeny</searchLink> ; <searchLink fieldCode="MH" term="%22Microbial+Sensitivity+Tests%22">Microbial Sensitivity Tests</searchLink> ; <searchLink fieldCode="MH" term="%22Spectrometry%2C+Mass%2C+Matrix-Assisted+Laser+Desorption-Ionization%22">Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization</searchLink> ; <searchLink fieldCode="MH" term="%22Drug+Resistance%2C+Bacterial%22">Drug Resistance, Bacterial</searchLink> ; <searchLink fieldCode="MH" term="%22Genome%2C+Bacterial%22">Genome, Bacterial</searchLink>
– Name: Abstract
  Label: Abstract
  Group: Ab
  Data: Peribacillus frigoritolerans is a bacterial species commonly found in the environment and used as a plant-growth promoter and biocontrol agent in agriculture. Recent evidence has proven that Peribacillus spp. are also able to cause severe infections in humans, thus emerging as new human pathogens. In this study, for the first time, 10 P. frigoritolerans strains were isolated from human samples (both superficial and sterile deep body sites) and characterized in terms of morphology, lifestyle, genetics, and virulence. The molecular identification by MALDI-TOF mass spectrometry and 16S rRNA gene sequencing was inconclusive, while whole-genome sequencing was effective in properly identifying isolates within the species P. frigoritolerans. The pangenome analysis provided an overview of the virulence potential of P. frigoritolerans, revealing the presence of genes involved in antibiotic resistance and toxin/exoenzyme production. Phenotypically, the strains displayed different features and behaviors, indicating strain-specific properties and high intra-species variability. A part of the strains exhibited virulence factors, being able to swim and swarm, form biofilms, and produce enzymes and toxins. Antibiotic susceptibility testing revealed resistance to ampicillin for all strains and resistance to erythromycin and clindamycin for some of them. Antimicrobial activity against Gram-positive bacteria and fungi was demonstrated, further corroborating the presence of putative bacteriocin/antimicrobial peptide-encoding genes. An association between the overall virulence potential and infection site/severity was hypothesized. Altogether, these findings highlight the extreme diversity within the species, reveal the strain-dependent pathogenic potential of P. frigoritolerans, and support its role as a candidate human pathogen.<br />Importance: This study provides insights into the infectious role of Peribacillus frigoritolerans, an almost unknown bacterial species with agrobiotechnological potential but no history of human infections. This is the first report of P. frigoritolerans isolation from human clinical samples. Ten P. frigorit-olerans strains were herein characterized for their morphology, lifestyle, genetics, and virulence, highlighting an extreme intra-species variability and the potential to act as pathogens in humans. Importantly, this study points out the need for unconventional methods for proper identification of this species, since traditional techniques result inconclusive. Resistance to commonly prescribed antibiotics was also evidenced, confirming the importance of antimicrobial testing on clinical iso-lates. This study lays the foundation for a more in-depth characterization of Peribacillus spp. in the clinical context.
– Name: Abstract
  Label: Competing Interests
  Group: Ab
  Data: The authors declare no conflict of interest.
– Name: Ref
  Label: References
  Group: RefInfo
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(PMID: <searchLink fieldCode="PM" term="%2232427907%22">32427907)</searchLink><br />Front Microbiol. 2018 Aug 17;9:1946. (PMID: <searchLink fieldCode="PM" term="%2230174669%22">30174669)</searchLink><br />Nat Commun. 2019 May 16;10(1):2182. (PMID: <searchLink fieldCode="PM" term="%2231097708%22">31097708)</searchLink><br />Biocontrol Sci. 2021;26(2):67-74. (PMID: <searchLink fieldCode="PM" term="%2234092716%22">34092716)</searchLink><br />Curr Microbiol. 2023 Jan 20;80(2):80. (PMID: <searchLink fieldCode="PM" term="%2236662359%22">36662359)</searchLink><br />J Appl Microbiol. 2024 Apr 1;135(4):. (PMID: <searchLink fieldCode="PM" term="%2238486365%22">38486365)</searchLink><br />Biotechnol J. 2024 Jan;19(1):e2300330. (PMID: <searchLink fieldCode="PM" term="%2238180313%22">38180313)</searchLink><br />Int J Syst Evol Microbiol. 2020 Jan;70(1):406-438. (PMID: <searchLink fieldCode="PM" term="%2231617837%22">31617837)</searchLink><br />Front Microbiol. 2024 Jul 03;15:1415400. 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(PMID: <searchLink fieldCode="PM" term="%2236823356%22">36823356)</searchLink><br />Nucleic Acids Res. 2022 Jan 7;50(D1):D912-D917. (PMID: <searchLink fieldCode="PM" term="%2234850947%22">34850947)</searchLink><br />Pathogens. 2022 Oct 18;11(10):. (PMID: <searchLink fieldCode="PM" term="%2236297260%22">36297260)</searchLink><br />Access Microbiol. 2025 Jan 14;7(1):. (PMID: <searchLink fieldCode="PM" term="%2239810798%22">39810798)</searchLink><br />Microorganisms. 2023 Sep 05;11(9):. (PMID: <searchLink fieldCode="PM" term="%2237764079%22">37764079)</searchLink><br />Microbiol Resour Announc. 2022 May 19;11(5):e0015222. (PMID: <searchLink fieldCode="PM" term="%2235389269%22">35389269)</searchLink><br />J Comput Biol. 2012 May;19(5):455-77. (PMID: <searchLink fieldCode="PM" term="%2222506599%22">22506599)</searchLink><br />Sci Rep. 2022 Nov 7;12(1):18883. (PMID: <searchLink fieldCode="PM" term="%2236344604%22">36344604)</searchLink><br />J Hazard Mater. 2024 Jan 5;461:132539. (PMID: <searchLink fieldCode="PM" term="%2237717445%22">37717445)</searchLink><br />Proc Natl Acad Sci U S A. 1965 Sep;54(3):704-11. (PMID: <searchLink fieldCode="PM" term="%224956288%22">4956288)</searchLink><br />Nucleic Acids Res. 2018 Jul 2;46(W1):W278-W281. (PMID: <searchLink fieldCode="PM" term="%2229788290%22">29788290)</searchLink><br />J Bacteriol. 2023 Jun 27;205(6):e0013323. (PMID: <searchLink fieldCode="PM" term="%2237195186%22">37195186)</searchLink><br />Front Microbiol. 2023 Dec 08;14:1290697. (PMID: <searchLink fieldCode="PM" term="%2238143858%22">38143858)</searchLink><br />Front Microbiol. 2023 May 05;14:1127321. (PMID: <searchLink fieldCode="PM" term="%2237234535%22">37234535)</searchLink><br />Arch Microbiol. 2022 Feb 4;204(3):162. (PMID: <searchLink fieldCode="PM" term="%2235119529%22">35119529)</searchLink><br />Clin Infect Dis. 2007 Jan 15;44(2):280-6. 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  Data: <i>Keywords: </i>Peribacillus frigoritolerans; antibiotic resistance; genome analysis; identification; microbiological characterization; virulence potential
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  Data: <i>Date Created: </i>20260715 <i>Date Completed: </i>20260807 <i>Latest Revision: </i>20260923
– Name: DateUpdate
  Label: Update Code
  Group: Date
  Data: 20260923
– Name: PubmedCentralID
  Label: PubMed Central ID
  Group: ID
  Data: PMC13436373
– Name: DOI
  Label: DOI
  Group: ID
  Data: 10.1128/spectrum.00245-26
– Name: AN
  Label: PMID
  Group: ID
  Data: 42454910
PLink https://search.ebscohost.com/login.aspx?direct=true&site=eds-live&db=cmedm&AN=42454910
RecordInfo BibRecord:
  BibEntity:
    Identifiers:
      – Type: doi
        Value: 10.1128/spectrum.00245-26
    Languages:
      – Code: eng
        Text: English
    PhysicalDescription:
      Pagination:
        StartPage: e0024526
    Subjects:
      – SubjectFull: RNA, Ribosomal, 16S genetics
        Type: general
      – SubjectFull: Anti-Bacterial Agents pharmacology
        Type: general
      – SubjectFull: Virulence Factors genetics
        Type: general
      – SubjectFull: Biofilms growth & development
        Type: general
      – SubjectFull: Humans
        Type: general
      – SubjectFull: Whole Genome Sequencing
        Type: general
      – SubjectFull: Virulence
        Type: general
      – SubjectFull: Phylogeny
        Type: general
      – SubjectFull: Microbial Sensitivity Tests
        Type: general
      – SubjectFull: Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization
        Type: general
      – SubjectFull: Drug Resistance, Bacterial
        Type: general
      – SubjectFull: Genome, Bacterial
        Type: general
      – SubjectFull: Bacillaceae genetics
        Type: general
      – SubjectFull: Bacillaceae isolation & purification
        Type: general
      – SubjectFull: Bacillaceae classification
        Type: general
      – SubjectFull: Bacillaceae drug effects
        Type: general
      – SubjectFull: Gram-Positive Bacterial Infections microbiology
        Type: general
    Titles:
      – TitleFull: Identification and in-depth characterization of clinical isolates of Peribacillus frigoritolerans.
        Type: main
  BibRelationships:
    HasContributorRelationships:
      – PersonEntity:
          Name:
            NameFull: Calvigioni M
      – PersonEntity:
          Name:
            NameFull: Rossi V
      – PersonEntity:
          Name:
            NameFull: Celandroni F
      – PersonEntity:
          Name:
            NameFull: Barnini S
      – PersonEntity:
          Name:
            NameFull: Lupetti A
      – PersonEntity:
          Name:
            NameFull: Mazzantini D
      – PersonEntity:
          Name:
            NameFull: Ghelardi E
    IsPartOfRelationships:
      – BibEntity:
          Dates:
            – D: 04
              M: 08
              Text: 2026 Aug 04
              Type: published
              Y: 2026
          Identifiers:
            – Type: issn-electronic
              Value: 2165-0497
          Numbering:
            – Type: volume
              Value: 14
            – Type: issue
              Value: 8
          Titles:
            – TitleFull: Microbiology spectrum
              Type: main
ResultId 1