Abstract
As one of the main pathogens of periodontitis, Porphyromonas gingivalis often forms mixed biofilms with other bacteria or fungi under the gingiva, such as Candida albicans. Heme is an important iron source for P. gingivalis and C. albicans that supports their growth in the host. From the perspective of heme competition, this study aims to clarify that the competition for heme enhances the pathogenic potential of P. gingivalis during the interaction between P. gingivalis and C. albicans. Porphyromonas gingivalis single-species biofilm and P. gingivalis-C. albicans dual-species biofilm were established in a low- and high-heme environment. The results showed that the vitality of P. gingivalis was increased in the dual-species biofilm under the condition of low heme, and the same trend was observed under a laser confocal microscope. Furthermore, the morphological changes in P. gingivalis were observed by electron microscope, and the resistance of P. gingivalis in dual-species biofilm was stronger against the killing effect of healthy human serum and antibiotics. The ability of P. gingivalis to agglutinate erythrocyte was also enhanced in dual-species biofilm. These changes disappeared when heme was sufficient, which confirmed that heme competition was the cause of thepathogenicy change in P. gingivalis. Gene level analysis showed that P. gingivalis was in a superior position in the competition relationship by increasing the expression of heme utilization-related genes, such as HmuY, HmuR, HusA, and Tlr. In addition, the expression of genes encoding gingipains (Kgp, RgpA/B) was also significantly increased. They not only participate in the process of utilizing heme, but also are important components of the virulence factors of P. gingivalis. In conclusion, our results indicated that the pathogenic potential of P. gingivalis was enhanced by C. albicans through heme competition, which ultimately promoted the occurrence and development of periodontitis and, therefore, C. albicans subgingival colonization should be considered as a factor in assessing the risk of periodontitis.
Highlights
Periodontitis is one of the main causes of tooth loss (Hajishengallis et al, 2012)
We explored for the first time the role of heme competition between P. gingivalis and C. albicans, and it provides a new method to study the crosstalk between bacteria and fungus
In order to understand the interaction between C. albicans and P. gingivalis, we first analyzed the viability of the two types of microorganisms at 12, 24, 36, and 48 h under hypoxia with 0.1 μg/ml heme
Summary
Periodontitis is one of the main causes of tooth loss (Hajishengallis et al, 2012). As the sixth largest infectious disease in the world, it is closely related to systemic diseases such as rheumatoid arthritis, atherosclerosis, and Alzheimer’s disease (Kumar, 2013; Kassebaum et al, 2014; Hussain et al, 2015; Leech and Bartold, 2015; Singhrao et al, 2015). It has been found that Candida albicans, a pathogen of denture stomatitis, has an increased frequency of subgingival separation in patients with periodontitis (McManus et al, 2012; Sardi et al, 2012; Marsh and Zaura, 2017) It can form a mixed biofilm with P. gingivalis. Previous studies using animal models of periodontal disease have shown that dual-species biofilm is more pathogenic than single-species biofilm (Daep et al, 2011) This increase in pathogenicity may be due to the formation of more complex and orderly microbial communities or the interaction between microorganisms to promote the secretion of virulent proteins, which will increase the difficulty of clinical treatment (Peleg et al, 2010; Harriott and Noverr, 2011; Xu and Dongari-Bagtzoglou, 2015; Hajishengallis and Lamont, 2016; Rajendran et al, 2016). Further exploration of the molecular mechanisms of the interaction between P. gingivalis and C. albicans, especially the influence of C. albicans on periodontal pathogen P. gingivalis, will be conducive to a deepened understanding of the pathogenesis of periodontitis
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