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Comparative Study
. 2019 Dec 20;5(1):37.
doi: 10.1038/s41522-019-0110-9. eCollection 2019.

Comparison of Japanese and Indian intestinal microbiota shows diet-dependent interaction between bacteria and fungi

Siddhika Pareek #  1   2   3 , Takashi Kurakawa #  1   2 , Bhabatosh Das  4 , Daisuke Motooka  5 , Shuuichi Nakaya  6 , Temsunaro Rongsen-Chandola  7 , Nidhi Goyal  7 , Hisako Kayama  1   2   3 , Dylan Dodd  8 , Ryu Okumura  1   2   3 , Yuichi Maeda  1   2   9 , Kosuke Fujimoto  1   9 , Takuro Nii  1   2   9 , Takao Ogawa  1   2   9 , Tetsuya Iida  5   10 , Nita Bhandari  7 , Toshiyuki Kida  11 , Shota Nakamura  5 , G Balakrish Nair  4 , Kiyoshi Takeda  1   2   3
Affiliations
Comparative Study

Comparison of Japanese and Indian intestinal microbiota shows diet-dependent interaction between bacteria and fungi

Siddhika Pareek et al. NPJ Biofilms Microbiomes. .

Abstract

The bacterial species living in the gut mediate many aspects of biological processes such as nutrition and activation of adaptive immunity. In addition, commensal fungi residing in the intestine also influence host health. Although the interaction of bacterium and fungus has been shown, its precise mechanism during colonization of the human intestine remains largely unknown. Here, we show interaction between bacterial and fungal species for utilization of dietary components driving their efficient growth in the intestine. Next generation sequencing of fecal samples from Japanese and Indian adults revealed differential patterns of bacterial and fungal composition. In particular, Indians, who consume more plant polysaccharides than Japanese, harbored increased numbers of Prevotella and Candida. Candida spp. showed strong growth responses to the plant polysaccharide arabinoxylan in vitro. Furthermore, the culture supernatants of Candida spp. grown with arabinoxylan promoted rapid proliferation of Prevotella copri. Arabinose was identified as a potential growth-inducing factor in the Candida culture supernatants. Candida spp. exhibited a growth response to xylose, but not to arabinose, whereas P. copri proliferated in response to both xylose and arabinose. Candida spp., but not P. copri, colonized the intestine of germ-free mice. However, P. copri successfully colonized mouse intestine already harboring Candida. These findings demonstrate a proof of concept that fungal members of gut microbiota can facilitate a colonization of the intestine by their bacterial counterparts, potentially mediated by a dietary metabolite.

Keywords: Microbiome; Symbiosis.

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Conflict of interest statement

Competing interestsThe authors declare no competing interests.

Figures

Fig. 1
Fig. 1. Comparison of fecal bacteria in healthy adults living in Japan and India.
a Relative abundances of the major genera. b Principal component analysis of fecal bacteria at the genus level. c Heatmap representing the relative abundances of bacterial species in genus Bacteroides and Prevotella. d Rarefaction curves. e Shannon index. n.s. not significant; ****p < 0.0001, ***p < 0.001, **p < 0.01, *p < 0.05.
Fig. 2
Fig. 2. Comparison of fecal fungi in healthy adults living in Japan and India.
a Relative abundances of the major genera. b Principal component analysis of fecal fungi at the genus level. c Heatmap representing the relative abundances of fungal species in genus Saccharomyces and Candida. d Rarefaction curves. e Shannon index. n.s. not significant; ****p < 0.0001; ***p < 0.001; *p < 0.05.
Fig. 3
Fig. 3. Co-utilization of arabinoxylan by Candida and Prevotella.
a, c, d Growth of P. copri (a), C. albicans (c), and C. tropicalis (d) in the presence or absence of 10 mM glucose, arabinoxylan (AX), starch, or carboxymethyl cellulose (CMC). The growth rate in the presence of AX and glucose was statistically compared. b, e, f Growth response of P. copri (b), C. albicans (e), and C. tropicalis (f) in the presence or absence of 10 mM glucose or the indicated concentrations of AX at 72 h. (−) is base media alone without any carbon source. n.s. not significant, n.d. not detected. ****p < 0.0001; ***p < 0.001; **p < 0.01.
Fig. 4
Fig. 4. Promotion of Prevotella growth by the metabolites produced by Candida.
Growth of P. copri JCM 13464 (a) and isolates from Indian feces (b) in the presence of glucose, AX, and C. tropicalis- or C. albicans-supernatants from cultures grown in AX. (−) is base media alone without any carbon source. Results of statistical comparison between C. albicans and C. tropicalis-supernatants from cultures grown in AX with AX alone are shown. All the graphs show the mean ± SD of three independent experiments. n.s. not significant. ****p < 0.0001, ***p < 0.001, **p < 0.01, *p < 0.05.
Fig. 5
Fig. 5. Identification of arabinose generated from Candida-dependent arabinoxylan metabolism.
a HPLC chromatograms of standards (upper: xylulose, xylose, xylobiose, xylotriose, and arabinose) and the C. albicans culture supernatant (lower). b TLC analyses of the C. albicans culture supernatant. Lane 1: arabinose (A); Lane 2: xylose (X1), xylobiose (X2), xylotriose (X3), xylotetraose (X4), xylopentaose (X5) and xylohexaose (X6); Lane 3: yeast nitrogen base medium with AX; Lane 4: culture supernatant of C. albicans grown in the presence of AX. c Direct mass spectrometry analysis of the spot detected in TLC analysis (Lane 4). Mass spectra of negative control (−) and sample spot of the TLC plates used for C. albicans culture supernatant. A unique ion peak was observed at m/z 277 in the C. albicans supernatant sample. d MS/MS spectra of the precursor ion at m/z 277 in the C. albicans supernatant sample (upper), and for arabinose (middle) and xylose (lower). The MS/MS fragment patterns of the C. albicans supernatant sample were identical to those of xylose and arabinose. e Concentration of D-xylose and l-arabinose in the medium with AX (−) and Candida culture supernatants with AX. C.T., C. tropicalis; C.A, C. albicans. Data are shown as means ± SD from three independent experiments. n.d. not detected.
Fig. 6
Fig. 6. In vitro growth of Candida and Prevotella in response to monosaccharides.
a–g Growth of C. albicans JCM 1542 (a), C. tropicalis JCM 1541 (b), C. albicans isolated from Indian feces (c), C. tropicalis isolated from Indian feces (d), C. glabrata isolated from Indian feces (e), P. copri JCM 13464 (f), and P. copri isolated from Indian feces (g) in the presence of 10 mM glucose, d-xylose or l-arabinose. Data from three independent experiments are shown as means ± SD. Statistical comparison between glucose and d-xylose (a–e) and between glucose and l-arabinose (f, g) is shown. n.s. not significant. ****p < 0.0001, **p < 0.01, *p < 0.05.
Fig. 7
Fig. 7. In vivo interaction of Prevotella and Candida in colonization of the mouse intestine.
a Schematic diagram of fungal and bacterial administration in the mouse intestine: germ-free BALB/c mice were administered with C. albicans (n = 4), P. copri (n = 5) or C. albicans + P. copri (n = 5). C. albicans was orally administered on day 0, and P. copri was orally administered on days 3–9. b–d Copy numbers of C. albicans (b, d) and P. copri (c, d) per gram of feces at the indicated time points (days) in mono- and co-administered groups. The number of mice, in which the copy numbers of the microorganisms were above the detection limit, is indicated on the graph. Data are representative of two independent experiments and are shown as means ± SD. The mean values are calculated based on copy numbers that were above the detection limit. e FISH using Candida-specific probe Dual 1249 (green), Prevotella-specific probe PRV392 (red), and 4′, 6-diamidino-2-phenylindole (DAPI; blue) on Carnoy’s fixed colon sections harvested from mice 26 days after the initial colonization. Scale bars, 10 µm.
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