Abstract
The female vaginal environment contains diverse microorganisms, and their interactions play significant roles in health and disease. Lactobacillus species are the predominant vaginal microorganisms in healthy women and relevant as a barrier to defense against pathogens, including Candida albicans. The yeast-to-hyphae transition is believed to be a determinant of C. albicans pathogenesis. In this study, we investigated the effects of vaginal isolates of L. crispatus (seven strains), L. gasseri (six strains), and L. jensenii (five strains) on growth, hyphal formation and virulence-related genes expression of C. albicans ATCC 10231. We found that the L. crispatus showed the most significant antimicrobial activities in microplate-based liquid medium assay (P < 0.05). All seven cell-free supernatants (CFS) from L. crispatus strains reduced the growth of C. albicans by >60%. The effects might be due to their productions of some secretory antimicrobial compounds in addition to H2O2 and organic acids. Furthermore, each of the CFS of Lactobacillus strains was found to significantly suppress the yeast-to-hyphae transition of C. albicans under hyphae-inducing conditions (RPMI 1640 medium supplemented with 10% fetal bovine serum). The hyphae inhibition rates of C. albicans treated by CFS from L. crispatus, L. gasseri, and L. jensenii were 88.3 ± 3.02%, 84.9 ± 6.0%, and 81.9 ± 6.2%, respectively. Moreover, the expression of hyphae-specific genes (ALS3, HWP1, ECE1, EAP1, and SAP5) and transcriptional regulatory genes (EFG1, TEC1, and NRG1) were analyzed using quantitative real-time PCR. The results demonstrated that L. crispatus CFS significantly down-regulated the expression of hyphae-specific genes ALS3 (0.140-fold)), HWP1 (0.075-fold), and ECE1 (0.045-fold), while up-regulated the expression of the negative transcriptional regulator gene NRG1 with 1.911-fold. The antimicrobial compounds from L. crispatus B145 against Candida growth were heat stable and protease resistance, but those against hyphal formation were partially sensitive to the same treatments. Our novel findings suggest that L. crispatus, a dominant Lactobacillus species associated with a healthy vagina, could strongly inhibit C. albicans growth and hyphal formation. L. crispatus might repress the expression of hyphae-specific genes (ALS3, HWP1, and ECE1) in a NRG1-dependent manner. Besides, L. crispatus B145 is highly worthwhile for probiotic investigation.
Highlights
Candida albicans is an opportunistic pathogen and the most prevalent fungal species of the human microbiota
The results showed that 15 of 18 (83.3%) Lactobacillus strains isolated from vaginal mucosa had inhibition activities on C. albicans growth (Table 2), among which more than half (8/15, 53.3%) had high inhibition activities ranked as +++
Comparing the different effects of Cell-Free Supernatant (CFS) on C. albicans gene expression, we found that all seven L. crispatus CFS significantly down-regulated the expression of agglutinin-like protein 3 (ALS3), HWP,1 and extent of cell elongation gene 1 (ECE1) genes (Figure 6), and there were no inter-strain difference except for gene hyphal wall protein 1 gene (HWP1) (Figures 7F–H)
Summary
Candida albicans is an opportunistic pathogen and the most prevalent fungal species of the human microbiota (da Silva Dantas et al, 2016). In some conditions this species can cause infections, such as VVC (Nobile and Johnson, 2015). VVC is responsible for a great morbidity among women of reproductive-age and significant burden to the health care system due to rising vaginitis-related health care costs. It is estimated that about 75% of all women at the childbearing age are afflicted by VVC at least once in their lifetime with ∼40–50% experiencing at least one additional episode of infection, ∼5–8% of women suffer from at least four recurrent VVC per year (Peters et al, 2014; Cassone, 2015)
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