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Prodigiosin of Serratia Marcescens ZPG19 Alters the Gut Microbiota Composition of Kunming Mice

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Prodigiosin of Serratia Marcescens ZPG19 Alters the Gut Microbiota Composition of Kunming Mice molecules Article Prodigiosin of Serratia marcescens ZPG19 Alters the Gut Microbiota Composition of Kunming Mice Xue Li 1 , Xinfeng Tan 1, Qingshuang Chen 1, Xiaoling Zhu 2, Jing Zhang 1,*, Jie Zhang 1,* and Baolei Jia 1,* 1 State Key Laboratory of Biobased Material and Green Papermaking, School of Bioengineering, Qilu University of Technology (Shandong Academy of Sciences), Jinan 250000, China; [email protected] (X.L.); [email protected] (X.T.); [email protected] (Q.C.) 2 Shandong Academy of Agricultural Sciences, Jinan 250000, China; [email protected] * Correspondence: [email protected] (J.Z.); [email protected] (J.Z.); [email protected] (B.J.) Abstract: Prodigiosin is a red pigment produced by Serratia marcescens with anticancer, antimalarial, and antibacterial effects. In this study, we extracted and identified a red pigment from a culture of S. marcescens strain ZPG19 and investigated its effect on the growth performance and intestinal micro- biota of Kunming mice. High-performance liquid chromatography/mass spectrometry revealed that the pigment had a mass-to-charge ratio (m/z) of 324.2160, and thus it was identified as prodigiosin. To investigate the effect of prodigiosin on the intestinal microbiota, mice (n = 5) were administered 150 µg/kg/d prodigiosin (crude extract, 95% purity) via the drinking water for 18 days. Administra- tion of prodigiosin did not cause toxicity in mice. High-throughput sequencing analysis revealed that prodigiosin altered the cecum microbiota abundance and diversity; the relative abundance of Desulfovibrio significantly decreased, whereas Lactobacillus reuteri significantly increased. This finding indicates that oral administration of prodigiosin has a beneficial effect on the intestinal microbiota of mice. As prodigiosin is non-toxic to mouse internal organs and improves the mouse intestinal Citation: Li, X.; Tan, X.; Chen, Q.; microbiota, we suggest that it is a promising candidate drug to treat intestinal inflammation. Zhu, X.; Zhang, J.; Zhang, J.; Jia, B. Prodigiosin of Serratia marcescens Keywords: gut microbiota; Kunming mice; pathologic visceral changes; prodigiosin; Serratia ZPG19 Alters the Gut Microbiota marcescens Composition of Kunming Mice. Molecules 2021, 26, 2156. https://doi. org/10.3390/molecules26082156 1. Introduction Academic Editor: Ricardo Calhelha Prodigiosin is a red microbial pigment with a tripyrrole ring structure [1–3]. It is mainly produced by Serratia marcescens [4,5], Pseudomonas, Actinomycetes, and some marine Received: 7 March 2021 bacteria [6–8]. Prodigiosin appears red under acidic and neutral conditions and yellow Accepted: 5 April 2021 under alkaline conditions [9,10]. As a bioactive substance, it has anticancer [11], antimalar- Published: 9 April 2021 ial [12], antibacterial [13,14], antigenic [15,16], and immunosuppressive effects. Prodigiosin inhibits algae growth and is used to control natural water pollution, such as that caused by Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in red tides and blooms [17]. Further, it is sensitive to light and is added to sunscreens and published maps and institutional affil- cosmetics to reduce UV damage to the skin [18]. Thus, prodigiosin has broad application iations. prospects in the fields of medicine, environmental management, and cosmetics. Prodigiosin can be classified into cycloprodigiosin, undecylprodigiosin, and meta- cycloprodigiosin (Figure1). Cycloprodigiosin produced by the marine bacterium Pseu- doalteromonas denitrificans, promotes inducible nitric oxide synthase gene expression in interleukin-1β-stimulated hepatocytes [19]. Undecylprodigiosin, produced by the marine Copyright: © 2021 by the authors. actinomycete Saccharopolyspora sp. novSP2-10, is considered a common precursor of the Licensee MDPI, Basel, Switzerland. prodigiosin family. It reduces microsclerotia formation by Verticillium dahliae in vitro [8]. This article is an open access article β distributed under the terms and Similar to undecylprodigiosin, metacycloprodigiosin selectively induces -catenin-mutant conditions of the Creative Commons tumor cell death [20]. Thus, prodigiosin exhibits species-specific functional differences. Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/). Molecules 2021, 26, 2156. https://doi.org/10.3390/molecules26082156 https://www.mdpi.com/journal/molecules MoleculesMolecules 20212021, 26,, 26x FOR, 2156 PEER REVIEW 2 of2 14 of 13 FigureFigure 1. Structures 1. Structures of the of the cycloprodigiosin, cycloprodigiosin, undecylprodigiosin, undecylprodigiosin, and and metacycloprodigiosin. metacycloprodigiosin. PreviousPrevious studies studies on on prodigiosin prodigiosin havehave focused focused on on the the screening screening of high-yielding of high‐yielding strains, strains,optimization optimization of the of fermentation the fermentation process, process, separation separation and purification, and purification, and in and vitro in biologi-vitro cal activities; however, the effect of prodigiosin on the intestinal microbiota of mice has not biological activities; however, the effect of prodigiosin on the intestinal microbiota of mice been investigated. It has been shown that oral administration of lactate and pyruvate en- has not been investigated. It has been shown that oral administration of lactate and py‐ hances the immune response and strengthens the intestinal resistance to Salmonella infection ruvate enhances the immune response and strengthens the intestinal resistance to Salmo‐ in mice [21]. Extracellular polysaccharides, a metabolite of Bifidobacterium, significantly nella infection in mice [21]. Extracellular polysaccharides, a metabolite of Bifidobacterium, increased the growth of Lactobacillus and anaerobic bacteria and inhibited Enterobacter, Ente- significantly increased the growth of Lactobacillus and anaerobic bacteria and inhibited rococcus and Bacteroides fragilis [22]. All these studies suggest that microbial metabolites can Enterobacter, Enterococcus and Bacteroides fragilis [22]. All these studies suggest that micro‐ enhance intestinal microecological balance. As the intestinal microbiota is closely related to bial metabolites can enhance intestinal microecological balance. As the intestinal microbi‐ health, and metabolites are the material basis for the communication between the intestinal ota is closely related to health, and metabolites are the material basis for the communica‐ flora and the host [23], we investigated the effect of oral administration of prodigiosin on tion between the intestinal flora and the host [23], we investigated the effect of oral ad‐ health in mice. To this end, we screened a strain of S. marcescens and purified and identified ministrationits pigment. of Crudeprodigiosin prodigiosin on health extract in mice. was usedTo this to end, study we its screened effects on a mousestrain of health, S. mar and‐ cescenshistopathological and purified observation and identified and its intestinal pigment. microbiological Crude prodigiosin analysis extract were usedwas toused provide to studya scientific its effects basis on formouse the safetyhealth, of and orally histopathological administered prodigiosin.observation and intestinal micro‐ biological analysis were used to provide a scientific basis for the safety of orally adminis‐ tered2. Materials prodigiosin. and Methods 2.1. Isolation of S. marcescens 2. Materials and Methods S. marcescens was isolated from compost generated by aerobic composting of Flam- 2.1.mulina Isolation velutipes of S. marcescensresidue that was anaerobically fermented for biogas production (Dezhou, China)S. marcescens and was storedwas isolated at 25 ◦ C.from One compost gram of compostgenerated was by immersed aerobic composting in physiological of Flam saline‐ mulinafor 2 velutipes h. After residue serially that diluting was theanaerobically sample solution, fermented 200 µforL wasbiogas added production onto Luria–Bertani (Dezhou, China)(LB) agarand was containing stored 0.075at 25 g/L°C. One K2Cr gram2O7 for of isolation. compost Thewas medium’s immersed pH in wasphysiological adjusted to saline7.2 withfor 2 NaOH h. After solution, serially and diluting then thethe mediumsample solution, was autoclaved. 200 μL Thewas platesadded were onto incubated Luria– ◦ Bertaniat 30 (LB)C. Redagar colonies containing were 0.075 picked g/L K and2Cr2 continuouslyO7 for isolation. streaked The medium to obtainʹs pH a pure was strain.ad‐ justedThe to strain 7.2 with was NaOH named solution,S. marcescens and thenZPG19 the andmedium was was deposited autoclaved. in the The China plates Centre were for incubatedType Culture at 30 °C. Collection Red colonies (CCTCC were M picked 2019645). and Colony continuously morphology streaked was to observed obtain a under pure a strain.microscope The strain (Eclipse was named E200; Nikon, S. marcescens Tokyo, ZPG19 Japan), and and was cell morphologydeposited in was the China observed Centre under fora Type scanning Culture electron Collection microscope (CCTCC (SUPRA™ M 2019645). 55; Carl Colony Zeiss, morphology Jena, Germany). was observed un‐ der a microscope (Eclipse E200; Nikon, Tokyo, Japan), and cell morphology was observed 2.2. 16S rRNA Gene-based Phylogenetic Analysis under a scanning electron microscope (SUPRA™ 55; Carl Zeiss, Jena, Germany). Genomic DNA of ZPG19 was extracted from cell biomass cultivated in LB broth. The 0 2.2.nearly 16S rRNA full-length Gene‐ 16Sbased rRNA Phylogenetic gene was Analysis amplified using 27F (5 -AGAGTTTGATCCTGGCTCAG-
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