Recent Developments in Applied Microbiology and Biochemistry
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Recent Developments in Applied Microbiology and Biochemistry provides a comprehensive treatment and understanding on application oriented microbial concepts, giving readers insights into recent developments in microbial biotechnology and medical, agricultural and environmental microbiology.
- Discusses microbial proteomics and their importance in medical microbiology
- Explores emerging trends in the prevention of current global health problems, such as cancer and obesity
- Shows recent approaches in the production of novel enzymes from environmental samples by enrichment culture and metagenomics approaches
- Guides readers through the status and recent developments in analytical methods for the detection of foodborne microorganisms
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Recent Developments in Applied Microbiology and Biochemistry - Viswanath Buddolla
book.
Section 1
Medical Microbiology and Biochemistry
Chapter 1
Recent Findings of Lactobacillus Diversity and Their Functional Role in Vaginal Ecosystems
Subramanyam Dasari Medical Sciences Program, Indiana University School of Medicine, Bloomington, IN, United States
Abstract
The reproductive system of female lies at the core of humanity, which is an immensely complex process that leads to successful reproduction, that is, miraculous yet invariably successful. Microorganisms have always been associated with the human body and have an important influence on development, physiology, immunity, and nutrition. The female genital tract is a complex of microbial colonization that shows a prominent role in the development of either a healthy or diseased condition. This is certainly true for the female genital tract; especially, the vagina (birth canal) is characterized by the presence of Lactobacillus-dominated microbiota, which develops the first line of defense for the host by excluding invasive, nonindigenous organisms that may cause disease. Hence, the aim of this chapter is to update knowledge about the vaginal Lactobacillus species that comprise normal vaginal flora and influence of pathogenic interactions with various defense mechanisms. This chapter also summarizes that protective mechanism is induced by various vaginal Lactobacillus species through the secretion of various antimicrobial, antiviral, anticancer compounds and inhibitory substances like organic acids, H2O2, bacteriocin, and toll-like receptors (TLRs). This knowledge should be included in the clinical practice of gynecologists to improve patient care.
Keywords
Vaginal ecosystem; Lactobacillus; Probiotics; Antimicrobial; Antiviral
Outline
1.1Introduction
1.2Vaginal (Birth Canal) Microbial Community
1.3Lactobacillus-Dominated Vaginal Microbiota
1.4Geographical Diversity of Vaginal Lactobacillus
1.5Functional Diversity in Vaginal Lactobacillus
1.5.1Production of Inhibitory Substances
1.5.2Blocking of Adhesion Sites
1.5.3Lactobacillus Induced Immunity
1.5.4Lactobacillus—Antiviral Activity
1.5.5Lactobacillus in Cancer Treatment and Management
1.6Conclusion
References
1.1 Introduction
The microbial communities have evolved their relation and association with us over thousands of years and are critical to our survival. For example, we rely on some bacteria for the absorption of nutrients and for conditioning the innate immune response; however, now, we are beginning to understand the complex mechanisms of these mutually beneficial interactions. On the other hand, disturbances in that microbiome may result in disease as well, and thus, improved knowledge of this association is critical to a better understanding of both human health and illness (Martin, 2012). An enormous number of microorganisms, especially bacterial species, are known to colonize and form complex communities, or microbiota, at various sites within and on the human body (Ling et al., 2010). Growing evidence suggests that the composition and function of the microbiota in different human body habitats play a pivotal role in human development, physiology, immunity, and nutrition (Dethlefsen et al., 2007). Female genital tract is created by a succession of cavities such as the uterine cavity, endocervix, and vagina with the exterior through the vulvar cleft. These cavities allow the exteriorization of the menstrual flow; on the other hand, it is normally colonized by a complex mixture of indigenous microbial flora. In the female —the vagina—is important microbial habitats that harbor different species of bacteria, which are known to have important effects on health (Ling et al., 2010). Experimental and clinical studies have been devoted to elucidating the microbiota of the vagina and, to a lesser extent, the cervix and vulva (Dasari et al., 2016).
In 1892, Döderlein isolated an organism from vaginal specimen of normal pregnant woman, called Döderlein’s bacillus, which later he named Lactobacillus (Linhares et al., 2010). It is well established that these Lactobacillus species inhabit the vaginal tract and play an important role in the maintenance of health by significantly inhibiting the growth of other organisms through the production of various defense mechanisms (Cribby et al., 2008). Production of lactic acid, bacteriocins, and hydrogen peroxide has led to an abundance of research involving the ability of Lactobacillus to inhibit the growth of bacterial and fungal pathogens that commonly cause urogenital tract infections (Westbroek et al., 2010). Hence, we try to discuss more about the recent findings of Lactobacillus diversity and their functional role (antimicrobial, antiviral, anticancer, and immunomodulatory properties of lactic acid) in maintaining the women’s health management.
1.2 Vaginal (Birth Canal) Microbial Community
The lower female reproductive tract (the vagina and ectocervix) is composed of a stratified squamous epithelium and glandular cells that make mucus, which is bathed in mucus and colonized with a large diversity of microbial flora that can have either commensal (benefit of one of the organisms, without effect on the other), mutualistic (both organisms benefit), or parasitic (microbes profit at the expense of the host) nature (Tachedjian et al., 2017). The vaginal microbial ecosystem undergoes significant structural changes at various growth stages in woman’s life that are directly associated with hormone levels (estrogen) in the body (Hickey et al., 2012). First microbial colonization occurs during birth, when the infant is first exposed to her mother’s birth canal. At the age of 2–4 weeks, maternal hormones mediate the lowering of the vaginal pH through the production of glycogen, which is fermented by indigenous bacteria in vaginal epithelial cells. Due to this low pH, until several weeks after birth, Lactobacillus is the predominant flora in vagina of a newborn girl. Nearly neutral pH was maintained during childhood and colonized by a diverse group of aerobic and strictly anaerobic bacteria and is highly susceptible to a variety of bacterial pathogens. During the menstrual process, follicular development causes hormone (estrogen) production and is accompanied by a thickening of the vaginal epithelium and intracellular production of glycogen. Lactobacillus again become prominent in this condition and are capable of fermenting glycogen to lactic acid, and the associated acidification of the vaginal environment is characteristic of women reproductive age. Apart from Lactobacillus, a smaller number of yeasts and other bacterial species are also present and are more resistant to infection (Dasari et al., 2016; Hickey et al., 2012).
1.3 Lactobacillus-Dominated Vaginal Microbiota
Lactobacillus is the keystone species present in the microbiota of the birth canal. It is well established that the high number of Lactobacillus in the vagina is often considered as healthy
or normal
and low or absence considered as abnormal
condition. Lactobacillus is popularized as lactic acid-producing bacteria by fermenting glycogen secreted from follicular cells of the vaginal epithelium, resulting in an enhanced acidic environment (pH < 4.5) (Linhares et al., 2010). The acidic environment of a healthy vagina prevents the growth of many potential pathogens. The most frequently detected Lactobacillus species are Lactobacillus iners, L. crispatus, and L. gasseri. Other species as L. jensenii, L. gallinarum, and L. vaginalis have also been identified in some women and approximately 10⁸ lactobacillus cells can be found per milliliter of vaginal fluid (Fredricks et al., 2005; Zhou et al., 2004). Lactobacillus forms a massive growth of biofilm, which tightly attaches to the vaginal epithelia surface, creating the first line of defense mechanism against potential pathogens. The vaginal fluid secreted from the stratified squamous epithelium contains specific organic acids, peroxides, and polypeptides that act as antibacterial agents against pathogenic or abnormal microbes (Dover et al., 2008). Vagina’s acid environment is an important defense mechanism against the proliferation of pathogens. When the flora of predominating Lactobacillus is reduced in the vaginal environment due to any reason, other bacteria (Megasphaera and Leptotrichia) start occupying and are capable of producing metabolites characterized by an unpleasant smell. Fig. 1.1 shows that the protective role of vaginal Lactobacillus through the production of various inhibitory substances and compounds blocks the adhesion sites and degradation of toxin receptors (Dasari et al., 2016). Table 1.1 summarizes the major findings on variations in composition of Lactobacillus species from female genital tract and their functional diversity. In the next sections, we are discussing more about the functional role of Lactobacillus in the management of female genital tract.
Fig. 1.1 Mode of action of vaginal Lactobacillus species: Lactobacillus are potentially inhibiting the pathogens in a direct manner by producing various compounds such as lactic acid, biosurfactants, hydrogen peroxide, and bacteriocin. In addition, they promote the integrity of the epithelium through stimulating mucus secretion and regulate the immune cells through inhibiting the bacterial and viral pathogens.
Table 1.1
1.4 Geographical Diversity of Vaginal Lactobacillus
In concern to the women’s health, the microbiome of vagina has not been extensively studied. Historically, L. acidophilus is the dominating species in human vagina, which motivates the scientific community to identify more therapeutic options for treatment of many diseases including cancer. It is an established fact that the composition of microbial flora is associated with various diseases; hence, it is important to know the diversity of Lactobacillus geographically and functionally. Previous studies clearly indicated that there is a global association between human microbial flora and different geographic locations for a better assessment of disease diagnosis and relative treatment of that population (Gupta et al., 2017). Table 1.2 summarizes the diversity of vaginal Lactobacillus in various countries.
Table 1.2
Lactobacillus species are known to be the predominant component of the healthy vaginal microbial flora, but some studies indicated that other species such as Gardnerella, Atopobium, Prevotella, Pseudomonas, or Streptococcus are predominant in some healthy women instead of Lactobacillus. Verstraelen et al. (2016) reported that vaginal microbiome of North American-Asian, North American white, and North American black women was dominated by Lactobacillus (51%–96%), but in Belgium population, vaginal microbiome was dominated by Bacteroides (34%) (Ravel et al., 2011; Verstraelen et al., 2016). However, a cohort study showed that vaginal Lactobacillus species isolated from South African women are similar to those identified in European populations, in which L. crispatus is related to a normal vaginal microbiota (Pendharkar et al., 2013). In another study, Zhou et al. demonstrated that Lactobacillus species were found to be more common in Caucasian women, while Atopobium is the dominated species in the communities of North American black women of reproductive age (Zhou et al., 2004). A vaginal microbial survey based on 16S rRNA in North American women from four ethnic groups (white, black, Hispanic, and Asian) elucidated the existence of five distinct groups of vaginal microbiome profiles: four were dominated by Lactobacillus species (L. crispatus, L. gasseri, L. iners, or L. jensenii), while the fifth contained lower proportions of lactic acid bacteria and higher proportions of obligate anaerobic bacteria (Ravel et al., 2011). Similar type of divergences in vaginal microbial flora has also been noticed between Belgian and Canadian women (Verstraelen et al., 2016) with L. crispatus. L. iners, and Prevotella prevailing in Belgian population and L. iners and L. jensenii in Canadian population.
1.5 Functional Diversity in Vaginal Lactobacillus
1.5.1 Production of Inhibitory Substances
Lactobacillus are known to produce various inhibitory substances and antimicrobial compounds to prevent vaginal infection caused by abnormal microbial flora (Dasari et al., 2014a). The antimicrobial compounds, such as bacteriocin-like substances, biosurfactants, and hydrogen peroxide, have been acting as an antagonistic effect of probiotic Lactobacillus strains against a variety of vaginal pathogens. Lactobacillus isolated from healthy vaginal swabs shows in vitro antimicrobial activity against cervicovaginal pathogens (Salmonella, Gardnerella, Enterococcus, and Neisseria) by the production of antimicrobial substances. The isolated Lactobacillus species are exhibiting probiotic characteristic and are more active under acidic conditions (Dasari et al., 2014b). The antimicrobial activity of Lactobacillus sp. is mainly due to the reduction in transmembrane potential (Δψ) and pH gradient produced by host cell immunity. Lactobacillus sp. produced antimicrobial peptides (bacteriocins), which are important defense mechanisms against competitive microorganisms. Bacteriocins are extracellular substances and exert their inhibitory activity through adsorption to specific receptors located on the surface of sensitive bacteria, followed by metabolic, biological, and morphological changes resulting in the killing of such bacteria (Daw and Falkiner, 1996). Vulvovaginal candidiasis, caused by Candida albicans, affects women at reproductive stage and is associated with the disruption of the healthy vaginal microbiota (Achkar and Fries, 2010). Recently, Wang et al. (2017) isolated nearly 18 Lactobacillus strains from healthy vagina and are tested to inhibit the growth of and hyphal formation of C. albicans. Interestingly, they found that the L. crispatus inhibited hyphal formation by downregulating the hypha-specific genes ALS3, HWP1, and ECE1 possibly through the overexpression of transcriptional repressor gene NRG1.
In another study, Dover et al. reported that the antimicrobials derived from vaginal probiotics were nontoxic to both animal and human vaginal tissue (Hillier et al., 1993). The production of lactic acid by vaginal Lactobacillus may be essential for the maintenance of a healthy ecosystem. Resulting acid pH prevents the excessive proliferation of potentially pathogenic microorganisms. It was confirmed by the O’Hanlon et al. (2013) that women with Lactobacillus-dominated vaginal microbiota have significantly more protection against infection than women with less vaginal Lactobacillus (O’Hanlon et al., 2013). Juárez Tomás et al. (2003) reported that L. acidophilus CRL 1259 isolated from the vagina inhibits the growth of uropathogenic Escherichia coli. Most of these Lactobacillus produce hydrogen peroxide, which possesses a defense mechanism against pathogens and seems to be less frequent in African-American women (Antonio et al., 1999).
1.5.2 Blocking of Adhesion Sites
Adherence of bacteria to epithelial cells has been shown to be an important factor in the colonization of mucous membranes. Competitive inhibition for bacterial adhesion sites on vaginal epithelial surfaces is another mechanism of action for Lactobacillus. Glycoproteins and carbohydrates produced by L. acidophilus and L. gasseri are responsible for adherence to the epithelial cells, which presumably were the targets of the competition observed between the Lactobacillus and the pathogenic microbes (Boris et al., 1998). Adhesion of human Lactobacillus species to mucin through various binding factors has been studied. Collagen-binding A precursor and aggregation-promoting factor-like proteins are suggested to participate on adhesion to HT-29, Caco-2, and HeLa cells. Interestingly, the extracellular proteins of L. plantarum Li69 and of L. salivarius Lv72 significantly inhibited the adhesion of Actinomyces neuii to HeLa cells (Martín et al., 2012). L. crispatus strains encode adhesion components called S-layer proteins that play a significant role on adherence of bacteria on HeLa cells. The potentiality of Lactobacillus to attach to the cells depends on various factors like the cell wall components of bacteria, cell receptors, and soluble proteins secreted by the host cells. However, more studies should be conducted on normal vaginal cell lines to elucidate the adhesion ability of Lactobacillus on epithelial cells and protection against bacterial and viral infections (Mousavi et al., 2017).
1.5.3 Lactobacillus Induced Immunity
The indigenous vaginal Lactobacillus of the genital tract are also involved in the prevention of microbial infection through innate and acquired immunity. Vaginal epithelial cells play a crucial role in the regulation of microbial infection by host-microbe interaction. In fact, epithelial cell secretions have some soluble factors with innate immunity (defensins, complement components, TLRs, nitric oxide, and phagocytic cells). Epithelial cells having TLRs recognize the pathogenic microbial components and trigger the development of antigen- specific acquired immunity by various signal transduction pathways (Dasari et al., 2016). A recent study using in vitro colonization of vaginal epithelial cell monolayers with common vaginal bacteria such as L. crispatus, Prevotella bivia, and Atopobium showed that these bacteria regulate the epithelial innate immunity in a species-specific manner (Doerflinger et al., 2014). Witkin et al. (2013) reported that d-lactic acid, present in vaginal secretions of women with L. crispatus-dominated microbiota, can inhibit expression of extracellular matrix metalloproteinase inducer (EMMPRIN) production. EMMPRIN induces matrix metalloproteinase 8 (MMP-8), which acts as a vaginal barrier more prone to upper genital infections associated to preterm birth (Witkin et al., 2013). Therefore, d-lactic acid production is an important factor in the protection against preterm delivery. Moreover, L. crispatus can also have beneficial effects via immunomodulation. For example, L. crispatus ATCC 33820 was shown to inhibit C. albicans in vitro by regulating the toll-like receptors (TLRs) 2/4, interleukin 8 (IL-8), and human β-defensin 2 and 3 expression in epithelial cells (HeLa) (Petrova et al., 2015).
1.5.4 Lactobacillus—Antiviral Activity
In vitro and in vivo experimental studies suggest that reduction in vaginal Lactobacillus content was identified as a predisposing factor for viral infections such as human papillomavirus (HPV) and herpes simplex virus (HSV) type. Recent prospective investigations demonstrated that there is a direct association between vaginal flora alterations and the occurrence of human immunodeficiency virus (HIV) infection (Zabihollahi et al., 2012). On the other hand, genital herpes and HPV infections are major risk factors for initiation and transmission of HIV via sexual contact (Atashili et al., 2008). Moreover, the HIV copy number in female genital tract discharge inversely correlates with vaginal Lactobacillus counts in bacterial flora (Sha et al., 2005). Therefore, Lactobacillus exhibit an important role both in preventing viral infections in the female and reducing the risk of infectious transmission to a healthy man. In vitro studies have revealed that hydrogen peroxide production by L. acidophilus strain shows a virucidal effect against HIV-1. Additionally, it has been reported that preincubation with different lactobacillus strains reduces the infection titer and thereby reduces the rate of infection of vesicular stomatitis virus (VSV) (Botić et al., 2007). Zabihollahi et al. (2012) evaluated that L. crispatus inactivated the 74% of HSV and HIV virion in coculture condition, suggesting that Lactobacillus may secrete a sort of molecules with viral neutralization activity (Zabihollahi et al., 2012). Recently, Mousavi et al. (2017) reported that L. crispatus (LC) shows potential antiviral activity against HSV-2 infection by either formation of LC microcolonies in the cell surface that could block HSV-2 receptor binding and prevent viral entry to cells during the initial stage of infection or entrapment of viral particles by direct interaction of L. crispatus with HSV-2 envelope (Mousavi et al., 2017). Galán and group determined the antiviral activity of Lactobacillus and Bifidobacterium species against rotavirus infection through the intracellular NSP4 protein production and Ca² + release (Galán et al., 2016).
1.5.5 Lactobacillus in Cancer Treatment and Management
Several in vitro and in vivo experimental studies suggest that the consumption of Lactobacillus sp. reduces the risk of cancers such as colon and cervical cancer. Recent reports demonstrated that there is an inverse association between cancer risk and yogurt and other fermented milk containing the probiotic Lactobacillus. Since most of the vaginal Lactobacillus species exhibit probiotic characters and are potentially used in the prevention and treatment of cancer through various mechanisms (Dasari et al., 2017). Sungur et al. (2017) reported that lyophilized EPS (L-EPS) produced by two vaginal Lactobacillus (L. gasseri) have anti-inflammatory effect on human cervical cancer cells (HeLa cells), and they inhibit the cell proliferation, by decreasing the production of TNF-α and increasing the IL-10 production (Sungur et al., 2017). Several in vitro studies demonstrated that common vaginal Lactobacillus (L. crispatus and L. gasser) exert cytotoxic effects on cervical tumor cells (HeLa cells), but not on normal cells, through the regulation of autophagy, cell cycle, and expression of oncogenes (Wang et al., 2017).
1.6 Conclusion
One of the most rapidly emerging researches is the management of vaginally acquired infections through its own normal flora—Lactobacillus. Several Lactobacillus species inhibit the growth of vaginally acquired pathogens by producing various compounds or reduce the adherence of pathogens to urogenital epithelial cells in culture and prevent pathogen colonization of the urogenital tract. Obviously, our knowledge about the vaginal microbiota dominating Lactobacillus and its functional output would contribute to an understanding of what truly constitutes normal
and abnormal.
It is expected that the application of this study will translate into better diagnostics and improved personalized treatments in female genital tract infections.
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