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Butyrate Production in Phylogenetically Diverse Firmicutes

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Butyrate Production in Phylogenetically Diverse Firmicutes mbt_244 Microbial Biotechnology (2011) doi:10.1111/j.1751-7915.2010.00244.x 1 Butyrate production in phylogenetically diverse 2 Firmicutes isolated from the chicken caecummbt_244 1..11 3 4 Venessa Eeckhaut,1* Filip Van Immerseel,1 present study indicates that butyrate producers 50 5 Siska Croubels,2 Siegrid De Baere,2 related to cluster XVI may play a more important role 51 6 Freddy Haesebrouck,1 Richard Ducatelle,1 in the chicken gut than in the human gut. 52 3 4 7 Petra Louis and Peter Vandamme 53 8 1Department of Pathology, Bacteriology and Avian Introduction 54 9 Diseases, Research Group Veterinary Public Health and 10 Zoonoses, and 2Department of Pharmacology, In the chicken gastrointestinal tract, the main sites of 55 11 Toxicology, Biochemistry and Organ Physiology, Faculty bacterial activity are the crop and the caeca and, to a 56 12 of Veterinary Medicine, Ghent University, Salisburylaan lesser extent, the small intestine. Lactobacillus spp. domi- 57 131 1 133, B-9820 Merelbeke, Belgium. nate the crop (Barnes et al., 1972; Watkins and Kratzer, 58 14 3Microbial Ecology Group, Rowett Institute of Nutrition 1983) and small intestinal tract (Lu et al., 2003), while the 59 15 and Health, University of Aberdeen, Greenburn Road, caecal microbiota are dominated by species of the 60 16 Bucksburn, Aberdeen AB219SB, UK. Clostridiales order, followed by Lactobacillales and Bacte- 61 17 4Laboratory of Microbiology, Faculty of Sciences, Ghent roidales (Dumonceaux et al., 2006). A molecular, culture- 62 18 University, K. L. Ledeganckstraat 35, B-9000 Ghent, independent study from Zhu and colleagues (2002) on the 63 19 Belgium. caecal microbiota of chickens identified 243 different 64 20 sequences, representing 50 phylogenetic groups or sub- 65 21 Summary groups of bacteria, with the majority of the caecal 66 sequences being near or above 95% identical to their 67 22 Sixteen butyrate-producing bacteria were isolated closest relatives in the database. Only about 10% of these 68 23 from the caecal content of chickens and analysed sequences corresponded with validly named species, 69 24 phylogenetically. They did not represent a coherent indicating that the knowledge of the intestinal microbiota 70 25 phylogenetic group, but were allied to four different of poultry is incomplete (Apajalahti et al., 2004; Bjerrum 71 26 lineages in the Firmicutes phylum. Fourteen strains et al., 2006). 72 27 appeared to represent novel species, based on a level The activity and composition of the caecal microbiota is 73 Յ 28 of 98.5% 16S rRNA gene sequence similarity largely influenced by diet-derived substrates that resist 74 29 towards their nearest validly named neighbours. The small intestinal digestion. Fermentation of these sub- 75 30 highest butyrate concentrations were produced by strates leads to formation of metabolites such as short- 76 31 the strains belonging to clostridial clusters IV and chain fatty acids (SCFAs) of which the concentration and 77 32 XIVa, clusters which are predominant in the chicken relative proportion is affected by the type and quantity of 78 33 caecal microbiota. In only one of the 16 strains tested, the available substrates (Wolin et al., 1999). The quanti- 79 34 the butyrate kinase operon could be amplified, while tatively most important SCFAs are acetic, propionic and 80 35 the butyryl-CoA : acetate CoA-transferase gene was butyric acid. Butyrate in particular is known to serve as the 81 36 detected in eight strains belonging to clostridial clus- direct energy source for the colonic epithelium (Roediger, 82 37 ters IV, XIVa and XIVb. None of the clostridial cluster 1980) and possesses anti-inflammatory properties result- 83 38 XVI isolates carried this gene based on degenerate ing from inhibition of the transcription factor NFkB activity 84 39 PCR analyses. However, another CoA-transferase (Place et al., 2005). In addition, butyric acid is capable to 85 40 gene more similar to propionate CoA-transferase was reinforce the colonic defence barrier by increasing the 86 41 detected in the majority of the clostridial cluster XVI production of mucins and host antimicrobial peptides 87 42 isolates. Since this gene is located directly down- (Barcelo et al., 2000; Schauber et al., 2003). Butyric acid 88 43 stream of the remaining butyrate pathway genes in also promotes the body weight of broilers and has an 89 44 several human cluster XVI bacteria, it may be inhibitory activity against Salmonella and Clostridium per- 90 45 involved in butyrate formation in these bacteria. The fringens (Leeson et al., 2005; Van Immerseel et al., 2005; 91 46 Hu and Guo, 2007; Timbermont et al., 2010). Little is 92 47 Received 4 September, 2010; accepted 22 November, 2010. *For 48 correspondence. E-mail [email protected]; Tel. (+32) known about the endogenous butyrate-producing capac- 93 49 92647361; Fax (+32) 92647789. ity in the lower intestinal tract of chickens, most likely 94 © 2010 The Authors Journal compilation © 2010 Society for Applied Microbiology and Blackwell Publishing Ltd mbt_244 2 V. Eeckhaut et al. 1 Table 1. Number of isolates within a butyrate-production range per sampled chicken and number of isolates consuming at least 2 mM acetate. 2 3 Acetate consumption 4 Butyrate production (mM) (Ն 2 mM) among all isolates 5 Butyrate Non-butyrate 6 Chicken (suffix) 0–2.0 2.1–5.0 5.1–10 10.1–15 > 15 producers producers 7 14-week-old layer (a) 37 16 8 4 0 12/28 0/37 8 4-week-old layer (b) 50 2 0 1 5 7/8 9/50 9 4-week-old broiler (c) 28 3 4 3 0 1/10 0/28 10 4-week-old broiler (d) 23 5 5 3 1 4/14 0/23 11 4-week-old broiler (e) 53 2 2 1 4 4/9 0/53 12 13 14 because only limited information is available on the iden- analysis of both types of fingerprints yielded comparable 53 15 tity and diversity of butyrate-producing bacteria in the results (data not shown) and 16 isolates with very distinct 54 16 chicken gut microbiota. Therefore the objective of the RAPD and REP-PCR fingerprints were selected for 55 17 present study was to isolate butyrate-producing bacteria further identification through 16S rRNA gene sequence 56 18 colonizing the caecum of chickens and to determine their analysis. Approximately 1300 bp of the 16S rRNA genes 57 19 pathway for butyrate production. were determined, compared with all sequence data in 58 public databases using the BLAST algorithm (Altschul 59 20 et al., 1990) and used for the construction of a phyloge- 22 60 21 Results netic tree (Fig. 1). The 16 isolates were distributed among 61 22 Isolation of butyrate-producing bacteria four clostridial clusters, cluster IV, XIVa, XIVb and XVI 62 (Collins et al., 1994), within the Firmicutes phylum. When 63 23 Dilutions of the caecal content were plated on M2GSC considering only validly named bacteria, three cluster IV 64 24 agar, since this medium was shown successful for the isolates (53-4c, 24-4c and 30-4c) were most closely 65 25 isolation of different types of butyrate producers from the related to Flavonifractor plautii (formerly Clostridium orbis- 66 26 human gut (Barcenilla et al., 2000). Sixty-five, 58, 38, 37 cindens) (Carlier et al., 2010) (97.7% and 95.7% 16S 67 27 and 62 colonies from a 14- and a 4-week-old layer pullet rRNA sequence similarity) and Pseudoflavonifractor cap- 68 28 and from 34-week-old broilers, respectively, were ran- illosus (formerly Bacteroides capillosus) (Carlier et al., 69 29 domly picked, grown overnight in M2GSC broth and 2010) (97.5% 16S rRNA sequence similarity) respec- 70 30 screened for fatty acid production. In accordance with the tively; one cluster IV isolate (40-4c) was most closely 71 31 study of Barcenilla and colleagues (2000), the cut-off related (97.8% 16S rRNA sequence similarity) to the 72 32 value was set at 2 mM butyrate for consideration as a butyrate-producing organism Subdoligranulum variabile; 73 33 butyrate producer. Twenty-six per cent of all tested iso- and two isolates (7-4c and 25-3b) were most closely 74 34 lates produced more than 2 mM butyrate, with the propor- related (91.5% and 92.7% 16S rRNA sequence similarity) 75 35 tion of butyrate-producing isolates varying between 14% to Eubacterium desmolans. From this cluster, isolate 76 36 and 43% for the five sampled chickens. The highest 25-3b was recently classified into a novel species within a 77 37 number of high-concentration butyrate producers novel genus, Butyricicoccus pullicaecorum (Eeckhaut 78 > 38 ( 15 mM) was isolated from the chickens, in which the et al., 2008). Three isolates (35-7e, 33-7e and 77-5d) 79 39 total number of butyrate producers was the lowest (b and were most closely related to members of the clostridial 80 40 e) (Table 1). At least 2 mM of the acetate present in the cluster XIVa, i.e. Anaerostipes caccae (94.5% 16S rRNA 81 41 M2GSC medium was consumed by 41% of all butyrate similarity), Eubacterium hallii (95.2% 16S rRNA similarity) 33 82 42 producers. All isolates from the 14-week-old layer and the and Clostridium populeti (92.5% 16S rRNA similarity) 83 43 three 4-week-old broiler chickens that consumed acetate respectively. In this cluster, the highest butyrate concen- 84 44 proved to be butyrate producers, in contrast with the iso- tration was produced by isolate 35-7e which was recently 85 45 lates from the 4-week-old layer where only 44% of the further characterized and classified into the novel species 86 46 acetate consumers were butyrate producers (Table 1).
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