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Akkermansia Muciniphila Is a Promising Probiotic

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Akkermansia Muciniphila Is a Promising Probiotic bs_bs_banner Minireview Akkermansia muciniphila is a promising probiotic Ting Zhang,1,2 Qianqian Li,1,2 Lei Cheng,3,4 Introduction Heena Buch1 and Faming Zhang1,2,* 1Medical Center for Digestive Diseases, the Second Several microbial species are getting increasing attention Affiliated Hospital of Nanjing Medical University, Nanjing for their role in modulating the gut microbiota. At present, 210011, China. many diseases and conditions have been reported to be 2Key Lab of Holistic Integrative Enterology, Nanjing closely related to gut microbiota (de Vos and de Vos, Medical University, Nanjing 210011, China. 2012), so it is of great interest to improve the host health 3Biogas Institute of Ministry of Agriculture and Rural by modulating the intestinal bacteria. Akkermansia muci- Affairs, Chengdu 610041, China. niphila (A. muciniphila) is a strict anaerobe recently iso- 4Center for Anaerobic Microbial Resources of Sichuan lated from human faeces and uses the mucin as the Province, Chengdu 610041, China. sole sources of carbon and nitrogen elements (Derrien et al., 2004). This mucin degrader is affected by the nutrients in the mucus layer located at a close distance Summary to the intestinal epithelial (Belkaid and Hand, 2014). Due to this unique function and its high universality and rich- Akkermansia muciniphila (A. muciniphila), an intesti- ness in almost all life stages, A. muciniphila has opened nal symbiont colonizing in the mucosal layer, is con- new avenues for the application in next-generation thera- sidered to be a promising candidate as probiotics. peutic probiotics (Collado et al., 2007; Derrien et al., A. muciniphila is known to have an important value 2008; Belzer and de Vos, 2012; Cani and de Vos, in improving the host metabolic functions and 2017). A series of studies have revealed that immune responses. Moreover, A. muciniphila may A. muciniphila regulated metabolic and immune func- have a value in modifying cancer treatment. How- tions, thus protecting mice from high-fat diets (Derrien ever, most of the current researches focus on the et al., 2011; Everard et al., 2013). Further analysis con- correlation between A. muciniphila and diseases, firmed A. muciniphila can degrade mucin and exert com- and little is known about the causal relationship petitive inhibition on other pathogenic bacteria that between them. Few intervention studies on degrade the mucin (Belzer and de Vos, 2012). These A. muciniphila are limited to animal experiments, findings provide a rationale for A. muciniphila to become and limited studies have explored its safety and effi- a promising probiotic. However, products containing cacy in humans. Therefore, a critical analysis of the A. muciniphila are currently not available worldwide. The current knowledge in A. muciniphila will play an exact mechanism underlying A. muciniphila interacts important foundation for it to be defined as a new with host remains unknown. Based on previous human beneficial microbe. This article will review the bacte- and animal studies, extensive assessment for riological characteristics and safety of A. muciniphila is still needed. Here, we will summarize A. muciniphila, as well as its causal relationship with and provide the updated information on the bacteriologi- metabolic disorders, immune diseases and cancer cal characteristics, safety, pathogenicity, antibiotic resis- therapy. tance of A. muciniphila and its effects on host health and diseases. Received 13 February, 2019; revised 2 April, 2019; accepted 4 April, 2019. *For correspondence. E-mail [email protected]; Tel. Characteristics of A. muciniphila +86 25 58509883; Fax +86 25 58509931. Microbial Biotechnology (2019) 0(0), 1–17 Akkermansia muciniphila is a bacterium of oval shape, doi:10.1111/1751-7915.13410 strictly anaerobic, non-motile and gram-negative and Funding Information This work was supported by National Natural Science Foundation of forms no endospores (Fig. 1). It was historically discov- China (NO. 81873548). The funding source had no role in the ered in 2004 at Wageningen University of the Nether- design of the study, collection, analysis and interpretation of data lands when searching for a new mucin-degrading and in writing the manuscript. ª 2019 The Authors. Microbial Biotechnology published by John Wiley & Sons Ltd and Society for Applied Microbiology. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. 2 T. Zhang et al. microbe in human faeces (Derrien et al., 2004). Akker- eventually reaches the same level as that in healthy mansia muciniphila is the first member and the only rep- adults (Collado et al., 2007; Derrien et al., 2008), but resentative of the phylum Verrucomicrobia in the human gradually decreases in the elderly (Collado et al., 2007). gut (Miller and Hoskins, 1981; Derrien et al., 2010), Previous phylogenetic and metagenomic studies based which is relatively easy to detect (Rajilic-Stojanovic and on hundreds of subjects have found that A. muciniphila de Vos, 2014). The genome of A. muciniphila strain is one of the top 20 most abundant species detectable MucT (=ATCC BAA-835T=CIP 107961T) involves one in the human gut (Collado et al., 2007, 2012; Qin et al., circular chromosome of 2.66 Mbp, which shared a lim- 2010; Arumugam et al., 2011; Thomas et al., 2014; Drell ited number of genes (29%) with its closest relatives in et al., 2015). In addition, A. muciniphila is reported to be the Verrucomicrobia phylum (van Passel et al., 2011). present in human milk (Collado et al., 2008). Human Recently, Guo et al. (2017) reported a high genetic milk can act as a carrier for the transfer of A. muciniphila diversity of A. muciniphila by whole-genome sequencing, from mothers to infants, thereby explaining its presence with 5644 unique proteins assembling a flexible open in the gastrointestinal tract of newborn infants (Collado pangenome. They further classified A. muciniphila into et al., 2007). At this life stage, A. muciniphila can suc- three species-level phylogroups, which demonstrated dif- cessfully colonize the gastrointestinal tract with the ferent function features. active acid resistance system and the ability to degrade It is widely distributed in the intestines of human and human milk oligosaccharides in newborn infants’ stom- animals (Belzer and de Vos, 2012; Lagier et al., 2015). ach (Bosscher et al., 2001). Akkermansia muciniphila was originally classified as a strictly anaerobic bacterium, but a recent study found Culturing A. muciniphila that it can tolerate low levels of oxygen, with an oxygen reduction capacity to be 2.26 Æ 0.99 mU mgÀ1 total pro- Akkermansia muciniphila is divided into three species- tein (Ouwerkerk, et al., (2017b). This property is similar level phylogenetic groups with distinct metabolic fea- to some intestinal anaerobic colonizers such as Bac- tures, but current studies still focused on the strain MucT teroides fragilis and Bifidobacterium adolescentis, which (=ATCC BAA-835T=CIP 107961T) (Guo et al., 2017). could still survive after exposure to ambient air for 48 h. Akkermansia muciniphila is sensitive to oxygen, and its Akkermansia muciniphila is abundant in the host intesti- growth medium is animal-derived compounds. Therefore, nal mucosal layer, with a largest number in the caecum. the clinical application of A. muciniphila is very limited It is found to be ubiquitous in the guts of healthy adults due to these limitations in culture conditions. Ottman and infants, and accounts for 1–4% of the total gut et al. (2017a,b) established a genome-scale metabolic microbiota starting from early life (Derrien et al., 2008). model to evaluate the substrate utilization abilities of Akkermansia muciniphila is one of the normal gut A. muciniphila. It showed that A. muciniphila can utilize symbionts throughout our life (Collado et al., 2007). This the mucin-derived monosaccharides fucose, galactose bacterium can stably colonize the human gut within and N-acetylglucosamine. These additional mucin- 1 year after birth, and its abundance in the gut derived components might be needed for its optimal growth. Plovier et al. (2017) reported that A. muciniphila can be grown on a synthetic media, in which the mucin is replaced by a combination of glucose, N-acetylgluco- samine, peptone and threonine. This synthetic medium is capable of culturing A. muciniphila at the same effi- ciency as the mucin medium, while avoiding all com- pounds that are incompatible with humans. At the same time, A. muciniphila grown on synthetic media was con- firmed to be safe for human administration (Plovier et al., 2017). A recent study reported that the genome-scale metabolic model can be used to accurately predict growth of A. muciniphila on synthetic media (van der Ark et al., 2018). They found that glucosamine-6-phosphate (GlcN6P), which exists in the mucin and prompts the adaptation to the mucosal niche, is a necessity for A. muciniphila. Moreover, Ouwerkerk et al. (2017a,b) proposed an Fig. 1. Scanning electronic micrograph of Akkermansia muciniphila. fi fl The A. muciniphila strain was isolated from a healthy Chinese donor ef cient scalable work ow for the preparation and for FMT at China fmtBank. Bar represents 2 lm. preservation of viable cells of A. muciniphila under strict ª 2019 The Authors. Microbial Biotechnology published by John Wiley & Sons Ltd and Society for Applied Microbiology. Akkermansia muciniphila is a beneficial microbe 3 anaerobic conditions for therapeutic interventions. An beneficial by-products (Derrien et al., 2008). To date, anaerobic plating system was used in this process to there is no evidence that A. muciniphila alone causes quantify the recovery and survival of viable cells of pathogenicity; nevertheless, it is not known whether it A. muciniphila. The preserved A. muciniphila cells may cause diseases in synergy with other bacteria. showed very high stability with survival rate of 97.9 Æ Akkermansia muciniphila, as a gram-negative bac- 4.5% for over 1 year at À80°C in glycerol-amended terium, contains lipopolysaccharide, but it is not associ- medium.
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