1887

Abstract

A total of 27 isolates that could not be classified to the species level were obtained from soil samples from different locations in the contiguous United States and an agricultural water sample from New York. Whole-genome sequence-based average nucleotide identity (ANIb) showed that the 27 isolates form five distinct clusters; for each cluster, all draft genomes showed ANI values of <95 % similarity to each other and any currently described species, indicating that each cluster represents a novel species. Of the five novel species, three cluster with the clade and two cluster with . One of the novel species, designated sp. nov., contains two subclusters with an average ANI similarity of 94.9%, which were designated as subspecies. The proposed three novel species (including two subspecies) are sp. nov. (type strain FSL L7-0091=CCUG 74668=LMG 31917; maximum ANI 91.9 % to ), sp. nov. (type strain FSL L7-1519=CCUG 74666=LMG 31920; maximum ANI 87.4 % to subsp. ) and sp. nov. [subsp. (type strain FSL L7-1447=CCUG 74667=LMG 31919; maximum ANI 93.4 % to ) and subsp. (type strain FSL L7-0993=CCUG 74670=LMG 31918; maximum ANI 94.7 % to ). The two proposed novel species are sp. nov. (type strain FSL L7-1582=CCUG 74671=LMG 31921; maximum ANI value of 88.9 % to and 89.2 % to ) and sp. nov. (type strain FSL W9-0585=CCUG 74665=LMG 31922; maximum ANI value of 88.7 % to and 88.9 % to . ). is the first species isolated to date that is non-motile. All five of the novel species are non-haemolytic and negative for phosphatidylinositol-specific phospholipase C activity; the draft genomes lack the virulence genes found in pathogenicity island 1 (LIPI-1), and the internalin genes and , indicating that they are non-pathogenic.

Funding
This study was supported by the:
  • National Institute of Health US) (Award T32ES007271)
    • Principle Award Recipient: DanWeller
  • Center for Produce Safety (Award 2017CPS09)
    • Principle Award Recipient: MartinWiedmann
  • Center for Produce Safety (Award 2018CPS13)
    • Principle Award Recipient: MartinWiedmann
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.004795
2021-05-17
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/71/5/ijsem004795.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.004795&mimeType=html&fmt=ahah

References

  1. Seastone CV. Pathogenic organisms of the genus Listerella. J Exp Med 1935; 62:203 [View Article][PubMed]
    [Google Scholar]
  2. Seeliger HP. [Nonpathogenic listeriae: L. innocua sp. n. (Seeliger et Schoofs, 1977) (author's transl)]. Zentralbl Bakteriol Mikrobiol Hyg A 1981; 249:487–493[PubMed]
    [Google Scholar]
  3. Seeliger HP, Rocourt J, Schrettenbrunner A, Grimont P, Jones D. Listeria ivanovii sp. nov. Int J Syst Evol Microbiol 1984; 34:336–337
    [Google Scholar]
  4. Boerlin P, Rocourt J, Grimont F, Grimont PA, Jacquet C et al. Listeria ivanovii subsp. londoniensis subsp. nov. Int J Syst Evol Microbiol. 1992; 42:69–73
    [Google Scholar]
  5. Rocourt J, Grimont P. Notes: Listeria welshimeri sp. nov. and Listeria seeligeri sp. nov. Int J Syst Bacteriol 1983; 33:866–869 [View Article]
    [Google Scholar]
  6. Graves LM, Helsel LO, Steigerwalt AG, Morey RE, Daneshvar MI et al. Listeria marthii sp. nov., isolated from the natural environment, Finger Lakes National Forest. Int J Syst Evol Microbiol 2010; 60:1280–1288 [View Article][PubMed]
    [Google Scholar]
  7. Rocourt J, Boerlin P, Grimont F, Jacquet C, Piffaretti JC. Assignment of Listeria grayi and Listeria murrayi to a single species, Listeria grayi, with a revised description of Listeria grayi. Int J Syst Bacteriol 1992; 42:171–174 [View Article][PubMed]
    [Google Scholar]
  8. Bertsch D, Rau J, Eugster MR, Haug MC, Lawson PA et al. Listeria fleischmannii sp. nov., isolated from cheese. Int J Syst Evol Microbiol 2013; 63:526–532 [View Article][PubMed]
    [Google Scholar]
  9. den Bakker HC, Manuel CS, Fortes ED, Wiedmann M, Nightingale KK. Genome sequencing identifies Listeria fleischmannii subsp. coloradonensis subsp. nov., isolated from a ranch. Int J Syst Evol Microbiol 2013; 63:3257–3268 [View Article][PubMed]
    [Google Scholar]
  10. den Bakker HC, Warchocki S, Wright EM, Allred AF, Ahlstrom C et al. Listeria floridensis sp. nov., Listeria aquatica sp. nov., Listeria cornellensis sp. nov., Listeria riparia sp. nov. and Listeria grandensis sp. nov., from agricultural and natural environments. Int J Syst Evol Microbiol 2014; 64:1882–1889 [View Article][PubMed]
    [Google Scholar]
  11. Núñez-Montero K, Leclercq A, Moura A, Vales G, Peraza J et al. Listeria costaricensis sp. nov. Int J Syst Evol Microbiol 2018; 68:844–850 [View Article][PubMed]
    [Google Scholar]
  12. Doijad SP, Poharkar KV, Kale SB, Kerkar S, Kalorey DR et al. Listeria goaensis sp. nov. Int J Syst Evol Microbiol 2018; 68:3285–3291 [View Article][PubMed]
    [Google Scholar]
  13. Leclercq A, Moura A, Vales G, Tessaud-Rita N, Aguilhon C et al. Listeria thailandensis sp. nov. Int J Syst Evol Microbiol 2019; 69:74–81 [View Article][PubMed]
    [Google Scholar]
  14. Quereda JJ, Leclercq A, Moura A, Vales G, Gómez-Martín Ángel et al. Listeria valentina sp. nov., isolated from a water trough and the faeces of healthy sheep. Int J Syst Evol Microbiol 2020; 70:ijsem004494 [View Article][PubMed]
    [Google Scholar]
  15. Weller D, Andrus A, Wiedmann M, den Bakker HC. Listeria booriae sp. nov. and Listeria newyorkensis sp. nov., from food processing environments in the USA. Int J Syst Evol Microbiol 2015; 65:286–292 [View Article][PubMed]
    [Google Scholar]
  16. Leclercq A, Clermont D, Bizet C, Grimont PAD, Le Flèche-Matéos A et al. Listeria rocourtiae sp. nov. Int J Syst Evol Microbiol 2010; 60:2210–2214 [View Article][PubMed]
    [Google Scholar]
  17. Lang Halter E, Neuhaus K, Scherer S. Listeria weihenstephanensis sp. nov., isolated from the water plant Lemna trisulca taken from a freshwater pond. Int J Syst Evol Microbiol 2013; 63:641–647 [View Article][PubMed]
    [Google Scholar]
  18. Orsi RH, Wiedmann M. Characteristics and distribution of Listeria spp., including Listeria species newly described since 2009. Appl Microbiol Biotechnol 2016; 100:5273–5287 [View Article][PubMed]
    [Google Scholar]
  19. Nightingale K, Bovell L, Grajczyk A, Wiedmann M. Combined sigB allelic typing and multiplex PCR provide improved discriminatory power and reliability for Listeria monocytogenes molecular serotyping. J Microbiol Methods 2007; 68:52–59 [View Article][PubMed]
    [Google Scholar]
  20. Lessing MPA, Curtis GDW, Bowler ICJ. Listeria ivanovii infection. J Infect 1994; 29:230–231
    [Google Scholar]
  21. Centers for Disease Control and Prevention 2019; Preliminary incidence and trends of infections with pathogens transmitted commonly through food - Foodborne Disease Active Surveillance Network, 10 U.S. sites, 2015-2018. Available at. https://www.cdc.gov/mmwr/volumes/68/wr/mm6816a2.htm?s_cid=mm6816a2_w26 November 2019
  22. Gouin E, Mengaud J, Cossart P. The virulence gene cluster of Listeria monocytogenes is also present in Listeria ivanovii, an animal pathogen, and Listeria seeligeri, a nonpathogenic species. Infect Immun 1994; 62:3550–3553 [View Article][PubMed]
    [Google Scholar]
  23. Vázquez-Boland JA, Kuhn M, Berche P, Chakraborty T, Domínguez-Bernal G et al. Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 2001; 14:584–640 [View Article][PubMed]
    [Google Scholar]
  24. Liao J Exploration of ecological and evolutionary mechanisms underlying microbial biogeography and adaptation. ProQuest Dissertations and Theses, 257. Retrieved from https://search-proquest-com.proxy.library.cornell.edu/docview/2449464420?accountid=10267: Cornell University,Order No. 28029926; 2020
  25. Weller D, Brassill N, Rock C, Ivanek R, Mudrak E et al. Complex interactions between weather, and microbial and physiochemical water quality impact the likelihood of detecting foodborne pathogens in agricultural water. bioRxiv 2020
    [Google Scholar]
  26. U.S. Food and Drug Administration 2017; Bacteriological Analytical Manual. Chapter 10, Detection of Listeria monocytogenes in Foods and Environmental Samples, and Enumeration of Listeria monocytogenes in Foods Available at. https://wwwfdagov/food/laboratory-methods-food/bam-detection-and-enumeration-listeria-monocytogenes25 March 2020
  27. Liao J, Wiedmann M, Kovac J. Genetic stability and evolution of the sigB allele, used for Listeria sensu stricto subtyping and phylogenetic inference. Appl Environ Microbiol 2017; 83:e00306–00317 [View Article][PubMed]
    [Google Scholar]
  28. Desjardins P, Conklin D. NanoDrop microvolume quantitation of nucleic acids. J Vis Exp 2010; 45:e2565 [View Article][PubMed]
    [Google Scholar]
  29. Mardis E, McCombie WR. Library quantification: fluorometric quantitation of double-stranded or single-stranded DNA samples using the qubit system. Cold Spring Harb Protoc 2017; 2017:pdb. prot094730 [View Article][PubMed]
    [Google Scholar]
  30. Kovac J, Cummings KJ, Rodriguez-Rivera LD, Carroll LM, Thachil A et al. Temporal genomic phylogeny reconstruction indicates a geospatial transmission path of Salmonella cerro in the United States and a clade-specific loss of hydrogen sulfide production. Front Microbiol 2017; 8:737 [View Article][PubMed]
    [Google Scholar]
  31. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article][PubMed]
    [Google Scholar]
  32. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article][PubMed]
    [Google Scholar]
  33. Mikheenko A, Prjibelski A, Saveliev V, Antipov D, Gurevich A. Versatile genome assembly evaluation with QUAST-LG. Bioinformatics 2018; 34:i142–i50 [View Article][PubMed]
    [Google Scholar]
  34. Wood DE, Salzberg SL. Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol 2014; 15:R46 [View Article][PubMed]
    [Google Scholar]
  35. Chun J, Oren A, Ventosa A, Christensen H, Arahal DR et al. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 2018; 68:461–466 [View Article][PubMed]
    [Google Scholar]
  36. Pritchard L, Glover RH, Humphris S, Elphinstone JG, Toth IK. Genomics and taxonomy in diagnostics for food security: soft-rotting enterobacterial plant pathogens. Analytical Methods 2016; 8:12–24
    [Google Scholar]
  37. Galili T. dendextend: an R package for visualizing, adjusting and comparing trees of hierarchical clustering. Bioinformatics 2015; 31:3718–3720 [View Article][PubMed]
    [Google Scholar]
  38. Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol 2018; 36:996–1004 [View Article][PubMed]
    [Google Scholar]
  39. Parks DH, Chuvochina M, Chaumeil P-A, Rinke C, Mussig AJ et al. A complete domain-to-species taxonomy for bacteria and archaea. Nat Biotechnol 20201–8
    [Google Scholar]
  40. Chaumeil P-A, Mussig AJ, Hugenholtz P, Parks DH. GTDB-Tk: a toolkit to classify genomes with the genome taxonomy database. Bioninformatics 2020
    [Google Scholar]
  41. Abascal F, Zardoya R, Posada D. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 2005; 21:2104–2105 [View Article][PubMed]
    [Google Scholar]
  42. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article][PubMed]
    [Google Scholar]
  43. Letunic I, Bork P. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 2016; 44:W242–W5 [View Article][PubMed]
    [Google Scholar]
  44. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:1–14
    [Google Scholar]
  45. Tindall BJ, Rosselló-Móra R, Busse H-J, Ludwig W, Kämpfer P. Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol 2010; 60:249–266 [View Article][PubMed]
    [Google Scholar]
  46. Meier-Kolthoff JP, Hahnke RL, Petersen J, Scheuner C, Michael V et al. Complete genome sequence of DSM 30083 T, the type strain (U5/41 T) of Escherichia coli, and a proposal for delineating subspecies in microbial taxonomy. Stand Genomic Sciences 2014; 9:1–19
    [Google Scholar]
  47. Rodriguez-R LM, Konstantinidis KT. Bypassing cultivation to identify bacterial species. Microbe 2014; 9:111–118
    [Google Scholar]
  48. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article][PubMed]
    [Google Scholar]
  49. Kumar S, Tamura K, Nei M. MEGA: molecular evolutionary genetics analysis software for microcomputers. Comput Appl Biosci 1994; 10:189–191 [View Article][PubMed]
    [Google Scholar]
  50. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [View Article][PubMed]
    [Google Scholar]
  51. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 1980; 16:111–120 [View Article][PubMed]
    [Google Scholar]
  52. Kim M, Oh H-S, Park S-C, Chun J. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 2014; 64:346–351 [View Article][PubMed]
    [Google Scholar]
  53. Collins MD, Wallbanks S, Lane DJ, Shah J, Nietupski R et al. Phylogenetic analysis of the genus Listeria based on reverse transcriptase sequencing of 16S rRNA. Int J Syst Bacteriol 1991; 41:240–246 [View Article][PubMed]
    [Google Scholar]
  54. Czajka J, Bsat N, Piani M, Russ W, Sultana K et al. Differentiation of Listeria monocytogenes and Listeria innocua by 16S rRNA genes and intraspecies discrimination of Listeria monocytogenes strains by random amplified polymorphic DNA polymorphisms. Appl Environ Microbiol 1993; 59:304–308 [View Article][PubMed]
    [Google Scholar]
  55. Vos P, Garrity G, Jones D, Krieg NR, Ludwig W et al. Bergey’s Manual of Systematic Bacteriology: Volume 3: The Firmicutes Springer Science & Business Media; 2011
    [Google Scholar]
  56. International Organization for Standardization Microbiology of food and animal feeding stuffs—Horizontal method for the detection and enumeration of Listeria monocytogenes. ISO 11290-1:2017. Interational Organization for Standardization 2017
    [Google Scholar]
  57. Pagotto F, Daley E, Farber J, Warburton D. Isolation of Listeria monocytogenes from all food and environmental samples. Canada Health Products Food Branch Compendium of analytical methods: laboratory procedures of microbiological analytical of foods,[MFHPB 30] Ottawa; 2001
  58. Bécavin C, Bouchier C, Lechat P, Archambaud C, Creno S et al. Comparison of widely used Listeria monocytogenes strains EGD, 10403S, and EGD-e highlights genomic variations underlying differences in pathogenicity. mBio 2014; 5:e00969-14 [View Article][PubMed]
    [Google Scholar]
  59. International Organization for Standardization Microbiology of food, animal feed and water - Preparation, production, storage and performance testing of culture media. ISO 11133:2014. International Organization for Standardization; 2014
  60. Buxton R. Nitrate and nitrite reduction test protocols; 2011
  61. Moura A, Criscuolo A, Pouseele H, Maury MM, Leclercq A et al. Whole genome-based population biology and epidemiological surveillance of Listeria monocytogenes. Nat Microbiol 2016; 2:16185 [View Article][PubMed]
    [Google Scholar]
  62. Ragon M, Wirth T, Hollandt F, Lavenir R, Lecuit M et al. A new perspective on Listeria monocytogenes evolution. PLoS Pathog 2008; 4:e1000146 [View Article][PubMed]
    [Google Scholar]
  63. Doumith M, Buchrieser C, Glaser P, Jacquet C, Martin P. Differentiation of the major Listeria monocytogenes serovars by multiplex PCR. J Clin Microbiol 2004; 42:3819–3822 [View Article][PubMed]
    [Google Scholar]
  64. Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S et al. Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 2012; 13:1–11
    [Google Scholar]
  65. Alcock BP, Raphenya AR, TTY L, Tsang KK, Bouchard M et al. Card 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res 2019; 48:D517–D25
    [Google Scholar]
  66. Møretrø T, Schirmer BCT, Heir E, Fagerlund A, Hjemli P et al. Tolerance to quaternary ammonium compound disinfectants may enhance growth of Listeria monocytogenes in the food industry. Int J Food Microbiol 2017; 241:215–224 [View Article][PubMed]
    [Google Scholar]
  67. Arndt D, Marcu A, Liang Y, Wishart DS. PHAST, PHASTER and PHASTEST: tools for finding prophage in bacterial genomes. Brief Bioinform 2019; 20:1560–1567 [View Article][PubMed]
    [Google Scholar]
  68. Schwengers O, Barth P, Falgenhauer L, Hain T, Chakraborty T et al. Platon: identification and characterization of bacterial plasmid contigs in short-read draft assemblies exploiting protein sequence-based replicon distribution scores. Microb Genom 2020; 6: [View Article][PubMed]
    [Google Scholar]
  69. Lachica RV. Hemolytic activity reevaluation of putative nonpathogenic Listeria monocytogenes strains. Appl Environ Microbiol 1996; 62:4293–4295 [View Article][PubMed]
    [Google Scholar]
  70. Chiara M, Caruso M, D'Erchia AM, Manzari C, Fraccalvieri R et al. Comparative genomics of Listeria sensu lato: genus-wide differences in evolutionary dynamics and the progressive gain of complex, potentially pathogenicity-related traits through lateral gene transfer. Genome Biol Evol 2015; 7:2154–2172 [View Article][PubMed]
    [Google Scholar]
  71. Wilson IG. Occurrence of Listeria species in ready to eat foods. Epidemiol Infect 1995; 115:519–526 [View Article][PubMed]
    [Google Scholar]
  72. Tortorello ML. Indicator organisms for safety and quality—uses and methods for detection: minireview. J AOAC Int 2003; 86:1208–1217[PubMed]
    [Google Scholar]
  73. U.S. Food and Drug Administration Draft guidance-for industry, control of Listeria monocytogenes-in-ready to eat foods; 2017
  74. AOAC International Methods Committee Guidelines for the Validation of Microbiological Methods for Food and Environmental Surfaces Gaithersburg, MD; 2012
    [Google Scholar]
  75. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P et al. DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 2007; 57:81–91 [View Article][PubMed]
    [Google Scholar]
  76. Raengpradub S, Wiedmann M, Boor KJ. Comparative analysis of the sigma B-dependent stress responses in Listeria monocytogenes and Listeria innocua strains exposed to selected stress conditions. Appl Environ Microbiol 2008; 74:158–171 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.004795
Loading
/content/journal/ijsem/10.1099/ijsem.0.004795
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error