Diversity of Listeria species in urban and natural environments

Abstract

A total of 442 Listeria isolates, including 234 Listeria seeligeri, 80 L. monocytogenes, 74 L. welshimeri, 50 L. innocua, and 4 L. marthii isolates, were obtained from 1,805 soil, water, and other environmental samples collected over 2 years from four urban areas and four areas representing natural environments. Listeria spp. showed similar prevalences in samples from natural (23.4%) and urban (22.3%) environments. While L. seeligeri and L. welshimeri were significantly associated with natural environments (P ≤ 0.0001), L. innocua and L. monocytogenes were significantly associated with urban environments (P ≤ 0.0001). Sequencing of sigB for all isolates revealed 67 allelic types with a higher level of allelic diversity among isolates from urban environments. Some Listeria spp. and sigB allelic types showed significant associations with specific urban and natural areas. Nearest-neighbor analyses also showed that certain Listeria spp. and sigB allelic types were spatially clustered within both natural and urban environments, and there was evidence that these species and allelic types persisted over time in specific areas. Our data show that members of the genus Listeria not only are common in urban and natural environments but also show species- and subtype-specific associations with different environments and areas. This indicates that Listeria species and subtypes within these species may show distinct ecological preferences, which suggests (i) that molecular source-tracking approaches can be developed for Listeria and (ii) that detection of some Listeria species may not be a good indicator for L. monocytogenes.

Fig 1

Distribution of sample locations across New York State. The geographic distribution of all locations sampled in four urban and four natural areas across New York State in 2001 and 2002 is shown. Northerly direction and distance scale (km) as indicated.

Fig 2

Phylogenetic tree of unique sigB allelic types. Neighbor-joining tree rooted with Bacillus subtilis; branch length for B. subtilis collapsed (//) by a factor of 100 for display purposes. Bootstrap values were obtained from 2,000 replicates; bootstrap values of >70 are shown.

Fig 3

Listeria species isolation frequency by sample type. Prevalence of Listeria spp. (percentage of positive samples) in different sample types (soil, vegetation, water, sidewalk/floors, and human contact surfaces) collected from (A) natural and (B) urban environments (2001 and 2002).

Fig 4

Listeria species isolation frequency by season. Seasonal prevalence (average of 2001 and 2002 data) of each Listeria species expressed as the percentage of positive samples from natural (A) and urban (B) environments with the corresponding number of positives samples indicated. A total of 233, 338, and 336 samples from natural environments and 194, 376, and 328 samples from urban environments were collected during spring, summer, and autumn, respectively.

Fig 5

Spatial clustering of L. welshimeri and L. welshimeri allelic types AT14 and AT21 in the Catskill Mountains. Spatial distribution is shown for all sampling locations and all sample locations positive for Listeria spp. (A), sample locations positive for L. welshimeri and other Listeria spp. (B), sample locations positive for L. welshimeri allelic type 14 (“haplotype 14”) and sample locations positive for other allelic types (regardless of Listeria species) (C), and sample locations positive for L. welshimeri allelic type 21 (“haplotype 21”) and sample locations positive for other allelic types (D).