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Degradation of Bile Acids by Soil and Water Bacteria

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Degradation of Bile Acids by Soil and Water Bacteria microorganisms Review Degradation of Bile Acids by Soil and Water Bacteria Franziska Maria Feller 1,†, Johannes Holert 1,† , Onur Yücel 1 and Bodo Philipp 1,2,* 1 Institute for Molecular Microbiology and Biotechnology, University of Münster, Corrensstr. 3, 48149 Münster, Germany; [email protected] (F.M.F.); [email protected] (J.H.); [email protected] (O.Y.) 2 Fraunhofer Institute for Molecular Biology and Applied Ecology IME, Auf dem Aberg 1, 57392 Schmallenberg, Germany * Correspondence: [email protected]; Tel.: +49-251-833-9827; Fax: +49-251-833-8388 † Contributed equally. Abstract: Bile acids are surface-active steroid compounds with a C5 carboxylic side chain at the steroid nucleus. They are produced by vertebrates, mainly functioning as emulsifiers for lipophilic nutrients, as signaling compounds, and as an antimicrobial barrier in the duodenum. Upon excretion into soil and water, bile acids serve as carbon- and energy-rich growth substrates for diverse het- erotrophic bacteria. Metabolic pathways for the degradation of bile acids are predominantly studied in individual strains of the genera Pseudomonas, Comamonas, Sphingobium, Azoarcus, and Rhodococcus. Bile acid degradation is initiated by oxidative reactions of the steroid skeleton at ring A and degrada- tion of the carboxylic side chain before the steroid nucleus is broken down into central metabolic intermediates for biomass and energy production. This review summarizes the current biochemical and genetic knowledge on aerobic and anaerobic degradation of bile acids by soil and water bacteria. In addition, ecological and applied aspects are addressed, including resistance mechanisms against the toxic effects of bile acids. Citation: Feller, F.M.; Holert, J.; Keywords: steroid degradation; bile acids; bacterial metabolism; cholic; deoxycholic; chenodeoxycholic Yücel, O.; Philipp, B. Degradation of Bile Acids by Soil and Water Bacteria. Microorganisms 2021, 9, 1759. https://doi.org/10.3390/ 1. Bile Acids and Their Occurrence in the Environment microorganisms9081759 Bile acids, or bile salts in their de-protonated state, are surface-active steroid com- Academic Editor: Jason Ridlon pounds that serve many functions in the digestive tract of vertebrates [1,2] and as regulatory signaling compounds [3]. These functions and the interplay of bile acids with gastrointesti- Received: 30 June 2021 nal bacteria [4–10] are described in the accompanying review articles of this special issue. Accepted: 12 August 2021 The focus of this review is on the current knowledge about the metabolic pathways of soil Published: 17 August 2021 and water bacteria, which use bile acids as a carbon and energy source under aerobic and anaerobic conditions and their ecological and biotechnological implications. Publisher’s Note: MDPI stays neutral More than 90% of vertebrae bile acids are typically re-adsorbed from the intestine with regard to jurisdictional claims in during the enterohepatic cycle. The rest is released into the environment by feces and urine. published maps and institutional affil- For example, humans release 400–600 mg of bile acids per person and day [4], adding up iations. to about 180 g per year. A large input of bile acids into the environment originates from farm animals. 1 g of cow feces contains about 1 mg cholic acid and 3 mg deoxycholic acid, and 1 g chicken feces can contain up to 7.5 mg chenodeoxycholic acid [11]. Theoretically, this could lead to bile acid concentrations in the millimolar range of up to 20 mM when Copyright: © 2021 by the authors. animal excretions are used on agricultural land as fertilizer [12]. In accordance with that, Licensee MDPI, Basel, Switzerland. about 0.3 mM deoxycholic and about 0.5 mM chenodeoxycholic acid were detected in cow This article is an open access article and poultry manure-runoff simulations [13], and even in rivers up to 13 nM of lithocholic distributed under the terms and acid and up to 76 nM of deoxycholic acid were detectable [14]. Bile acids are also released conditions of the Creative Commons by aquatic vertebrates, functioning as signaling compounds [15,16]. Attribution (CC BY) license (https:// As a result of their widespread release by vertebrates, bile acids constitute a rich creativecommons.org/licenses/by/ nutrient source for many bacteria in soils and water, in particular near fecal pellets of 4.0/). Microorganisms 2021, 9, 1759. https://doi.org/10.3390/microorganisms9081759 https://www.mdpi.com/journal/microorganisms Microorganisms 2021, 9, x FOR PEER REVIEW 2 of 28 Microorganisms 2021, 9, 1759 2 of 29 As a result of their widespread release by vertebrates, bile acids constitute a rich nu- trient source for many bacteria in soils and water, in particular near fecal pellets of verte- brates and in manure-fertilized areas (Figure 1). In accordance with this, rapid chenodeox- vertebrates and in manure-fertilized areas (Figure1). In accordance with this, rapid chen- ycholic acid degradation was observed in soil slurries from agricultural fields that were odeoxycholic acid degradation was observed in soil slurries from agricultural fields that spiked with this bile acid [12]. Bacterial growth in enrichment cultures containing bile were spiked with this bile acid [12]. Bacterial growth in enrichment cultures containing acids as substrates inoculated with soil or freshwater usually occurs within 24–48 h and bile acids as substrates inoculated with soil or freshwater usually occurs within 24–48 h bile acid-degrading bacteria can readily be isolated from terrestrial and limnic habitats and bile acid-degrading bacteria can readily be isolated from terrestrial and limnic habi- [17–19]. Further supporting this, a recent study analyzing steroid degradation genes in tats [17–19]. Further supporting this, a recent study analyzing steroid degradation genes in metagenomesmetagenomes fromfrom diversediverse environmentsenvironments revealedrevealed thatthat soilssoils andand rhizosphere,rhizosphere, asas wellwell asas marinemarine andand selected selected freshwater freshwater environments, environments are, are prominent prominent habitats habitats for for steroid-degrading steroid-degrad- bacteriaing bacteria [20]. [20]. As bile As bile acids acids are highlyare highly reduced reduced and and carbon-rich carbon-rich compounds, compounds, they they provide pro- anvide attractive an attractive carbon- carbon and- energyand energy source, source, particularly particularly in nutrient-poor in nutrient-poor soils soils and and waters. wa- Pseudomonasters. Pseudomonas stutzeri stutzeriChol1 Chol1 has a molarhas a molar growth growth yield of yield about of 250about g dry 250 mass g dry per mass mol per cholic mol acidcholic under acidaerobic under aerobic conditions conditions [19]. This [19]. suggests This suggests that about that 25 molabout adenosine 25 mol adenosine triphosphate tri- (ATP)phosphate can be (ATP) derived can from be derived the degradation from the ofdegradation 1 mol cholic of acid,1 mol considering cholic acid, that considering 1 mol of ATPthat is1 mol required of ATP for is the required formation for the of 10 formation g of dry massof 10 [g21 of]. dry mass [21]. FigureFigure 1.1. ManureManure fertilizerfertilizer onon agriculturalagricultural fieldsfields asas aa sourcesource forfor bilebile salts,salts, whichwhich cancan bebe usedused asas aa carboncarbon andand energyenergy sourcesource byby heterotrophicheterotrophic bacteria. bacteria. In spite of their good degradability, bile acids can be used as paleontological mark- In spite of their good degradability, bile acids can be used as paleontological markers ers [22] in some environments where their degradation is hindered by adverse environ- [22] in some environments where their degradation is hindered by adverse environmental mental factors such as unfavorable pH, temperature, or salinity, desiccation, or a lack of factors such as unfavorable pH, temperature, or salinity, desiccation, or a lack of suitable suitable electron acceptors. electron acceptors. 2. Bacterial Bile Acid Degradation 2.1.2. Bacterial Diversity Bile of Bile Acid Acid-Degrading Degradation Bacteria 2.1. DiversityIn recent of years, Bile Acid many-Degrading bile acid-degrading Bacteria bacteria have been isolated from different environmentsIn recent suchyears, as many meadows, bile acid freshwater,-degrading and bacteria marine have habitats. been All isolated these strainsfrom different belong toenvironments the Proteobacteria such as or meadows, Actinobacteria. freshwater Among, and the marine Proteobacteria, habitats. All individual these strains strains belong of theto the genera ProteobacteriaSphingomonas or ,ActinobacteriaSphingobium, Novosphingobium. Among the Proteobacteria,(a-Proteobacteria; individual ([18 ,strai23])),nsCo- of mamonasthe genera, Azoarcus Sphingomonas, Zoogloea, Sphingobium(b-Proteobacteria;, Novosphingobium [18,24,25]), (Pseudomonasα-Proteobacteria;, Pseudoalteromonas ([18,23])), Co- andmamonasShewanella, Azoarcus(g-Proteobacteria;, Zoogloea (β-Proteobacteria; [17,19,26,27]) [18,24,25] have been), identifiedPseudomonas to be, Pseudoalteromonas able to degrade bileandacids. Shewanella Among (γ- theProteobacteria; Actinobacteria, [17,19,26,27] several members) have been of the identified genus Rhodococcus to be able to[28 degrade,29], as wellbile asacids. individual Among strains the Actinobacteria, from the genera severalThermomonospora members of, Amycolatopsisthe genus Rhodococcus[27], Dietzia [28,29],[18], Gordoniaas
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