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. 2012 Oct;80(10):3371-80.
doi: 10.1128/IAI.00449-12. Epub 2012 Jul 9.

Candida albicans and bacterial microbiota interactions in the cecum during recolonization following broad-spectrum antibiotic therapy

Katie L Mason  1 , John R Erb Downward, Kelly D Mason, Nicole R Falkowski, Kathryn A Eaton, John Y Kao, Vincent B Young, Gary B Huffnagle
Affiliations

Candida albicans and bacterial microbiota interactions in the cecum during recolonization following broad-spectrum antibiotic therapy

Katie L Mason et al. Infect Immun. 2012 Oct.

Abstract

Candida albicans is a normal member of the gastrointestinal (GI) tract microbiota of healthy humans, but during host immunosuppression or alterations in the bacterial microbiota, C. albicans can disseminate and cause life-threatening illness. The bacterial microbiome of the GI tract, including lactic acid bacteria (LAB), plays a vital role in preventing fungal invasion. However, little is known about the role of C. albicans in shaping the bacterial microbiota during antibiotic recovery. We investigated the fungal burdens in the GI tracts of germfree mice and mice with a disturbed microbiome to demonstrate the role of the microbiota in preventing C. albicans colonization. Histological analysis demonstrated that colonization with C. albicans during antibiotic treatment does not trigger overt inflammation in the murine cecum. Bacterial diversity is reduced long term following cefoperazone treatment, but the presence of C. albicans during antibiotic recovery promoted the recovery of bacterial diversity. Cefoperazone diminishes Bacteroidetes populations long term in the ceca of mice, but the presence of C. albicans during cefoperazone recovery promoted Bacteroidetes population recovery. However, the presence of C. albicans resulted in a long-term reduction in Lactobacillus spp. and promoted Enterococcus faecalis populations. Previous studies have focused on the ability of bacteria to alter C. albicans; this study addresses the ability of C. albicans to alter the bacterial microbiota during nonpathogenic colonization.

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Figures

Fig 1
Fig 1
C. albicans colonization of germfree and conventional mice. (A) Germfree mice were given a single oral gavage of C. albicans CHN1, and the GI organs were removed at days 7 and 21 postgavage. The pSI, dSI, cecum, and colon were removed at day 7 or day 21 and differentially cultured to determine C. albicans colonization. All germfree colonized mice had detectable C. albicans at all times points. (B to E) The GI organs of conventional mice were removed at day 7 and day 21 postgavage (C. albicans CHN1) with or without pretreatment with cefoperazone. The organs were differentially cultured to determine C. albicans CHN1 colonization. Untreated mice and cefoperazone-only mice had no detectable C. albicans CHN1 colonization. The error bars represent the standard errors of the mean. *, P < 0.05 versus untreated mice.
Fig 2
Fig 2
C. albicans colonization of the murine cecum does not result in histological inflammation. Histological H&E sections of the murine cecum were examined to look for evidence of inflammation during cefoperazone-induced microbiota disruption. All treatment groups (untreated, cefoperazone only, C. albicans only, and cefoperazone plus C. albicans) had no histological evidence of inflammation during microbiota disruption at day 7 (data not shown) and day 21 (A to D).
Fig 3
Fig 3
Cefoperazone and C. albicans alter bacterial diversity in the murine cecum. Rarefaction analysis was performed on the TRFs found in the T-RFLP analysis at days 7 (B) and 21 (D). The solid lines indicate the mean rarefied values, whereas the dashed lines indicate the standard errors (n = 8 per group). (A and C) Canonical correspondence analysis of the day 7 (A) and day 21 (C) communities; the data were constrained by treatment type. Both models were significant (P < 0.05 [anova.cca]), and both CCA1 and CCA2 were found to be significant axes (P < 0.05) at both time points.
Fig 4
Fig 4
Cefoperazone alters short-term bacterial diversity, but C. albicans alters bacterial diversity in the murine cecum long term. The cecum was removed and analyzed using T-RFLP. Rank abundance plots were constructed from TRFs in each of the experimental groups at day 7 (A) and day 21 (B). The error bars represent the standard errors of the mean, where the mean is pooled TRFs from individual mice within each experimental group. The Bray Curtis distance was determined to compare each experimental group at day 7 and day 21.
Fig 5
Fig 5
Rarefaction analysis of microbial communities in the murine cecum. The number of OTUs for each experimental treatment group was used to construct rarefaction curves from clone library data with an OTU definition of 97% (A and B) or 90% (C and D) sequence similarity. (E and F) Comparison of the cecal communities in untreated animals and in animals treated with cefoperazone alone, C. albicans alone, and cefoperazone plus C. albicans at day 7 (E) and day 21 (F) using an OTU definition of 97% similarity in the Bray-Curtis similarity metric; the results are displayed in dendrogram format.
Fig 6
Fig 6
Bacterial composition of the murine cecum during C. albicans colonization. Clone libraries were constructed to investigate the relative abundances of the bacteria in the murine cecum at day 7 (A and B) and day 21 (C and D). Bacterial populations are shown as percentages of the total 16S rRNA clones for each treatment group. Cefoperazone treatment in the presence or absence of C. albicans diminished Bacteroidetes populations in the cecum at day 7. At day 21, the presence of C. albicans during recovery from cefoperazone resulted in recovery of Bacteroidetes populations, while there was no recovery in cefoperazone-only mice.
Fig 7
Fig 7
C. albicans CHN1 during antibiotic treatment promotes E. faecalis growth in the murine cecum. (A and B) The cecum was removed at day 7 (A) and day 21 (B) postantibiotic and differentially cultured to determine total LAB colonization in untreated, cefoperazone-treated, C. albicans-only, or cefoperazone-plus-C. albicans mice (graphs). LAB colonies that grew on MRS-plus-azide agar were further identified, using colony PCR as described in Materials and Methods, and expressed as a fraction of the total LAB population in that group (pie charts). The error bars represent the standard errors of the mean (*, P < 0.05 compared to untreated mice). (C) E. faecalis and L. johnsonii were isolated from the cecum of a cefoperazone-treated mouse, and their in vitro susceptibilities to cefoperazone were determined. The error bars represent the standard errors of the mean. No statistical significance was found between any of the groups (n = 3 to 6/group).
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