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. 2016 Oct 26:6:36157.
doi: 10.1038/srep36157.

Opportunistic fungal pathogen Candida glabrata circulates between humans and yellow-legged gulls

Mohammed Hashim Al-Yasiri  1 , Anne-Cécile Normand  2 , Coralie L'Ollivier  1   2 , Laurence Lachaud  3   4 , Nathalie Bourgeois  3 , Stanislas Rebaudet  1 , Renaud Piarroux  1   2 , Jean-François Mauffrey  5 , Stéphane Ranque  1   2
Affiliations

Opportunistic fungal pathogen Candida glabrata circulates between humans and yellow-legged gulls

Mohammed Hashim Al-Yasiri et al. Sci Rep. .

Abstract

The opportunistic pathogenic yeast Candida glabrata is a component of the mycobiota of both humans and yellow-legged gulls that is prone to develop fluconazole resistance. Whether gulls are a reservoir of the yeast and facilitate the dissemination of human C. glabrata strains remains an open question. In this study, MLVA genotyping highlighted the lack of genetic structure of 190 C. glabrata strains isolated from either patients in three hospitals or fecal samples collected from gull breeding colonies located in five distinct areas along the French Mediterranean littoral. Fluconazole-resistant isolates were evenly distributed between both gull and human populations. These findings demonstrate that gulls are a reservoir of this species and facilitate the diffusion of C. glabrata and indirect transmission to human or animal hosts via environmental contamination. This eco-epidemiological view, which can be applied to other vertebrate host species, broadens our perspective regarding the reservoirs and dissemination patterns of antifungal-resistant human pathogenic yeast.

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Figures

Figure 1
Figure 1. STRUCTURE clustering (admixture) in which each isolate is represented by a single vertical line that is partitioned into K = 2 colored segments.
The segment length represents the individual’s estimated membership fractions in cluster 1 (red) and cluster 2 (green). Isolates with multiple colors have admixed genotypes from each cluster.
Figure 2
Figure 2. Minimum spanning tree of the 190 C. glabrata isolates collected from gulls or patients.
Each node represents a unique MLVA genotype, and the various colors of the nodes indicate the study site. The single-locus variants are linked with thick solid lines, double-locus with thin solid line, while the triple-locus variants are linked with dashed lines. The two genetic clusters identified using STRUCTURE software are outlined in red (cluster 1; n = 101) and green (cluster 2; n = 89).
Figure 3
Figure 3. Map of the three cities, Montpellier, Nîmes and Marseille, and the yellow-legged gulls’ breeding colonies in the Mediterranean areas where isolates were sampled.
The nodes indicate the relative number of isolates sampled in the respective region. Pie chart colors correspond to the proportion of two genetic clusters of the 190 Candida glabrata isolates at each site. C. glabrata population differentiation between study sites was measured via calculation of pairwise FST. Statistically significant FST values are indicated in bold. The locations of the yellow-legged gulls’ breeding colonies are abbreviated as: PB = lagoon of Pierre Blanche; PF = Palavas-les-Flots; GM = La Grande-Motte; FR = Frioul Archipelago; and RI = Riou Archipelago). [This map was created on the open source QGIS Geographic Information System software version 2.12.1-Lyon (http://qgis.osgeo.org), using an open license shapefile of French departments obtained from IGN (http://professionnels.ign.fr/geofla)].
Figure 4
Figure 4. MLVA-based minimum spanning tree of 54 C. glabrata isolates from Marseille hospital patients and gulls from the Riou and Frioul archipelagos off the coast of Marseille.
In vitro resistance to the antifungal fluconazole was found in 9 and 14 isolates from gull and human hosts, respectively. Blue nodes indicate human isolates; green nodes indicate gull isolates; dark colors indicate resistance to fluconazole and light colors indicate susceptibility to fluconazole.
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