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. 2019 Mar 13;83(2):e00054-18. doi: 10.1128/MMBR.00054-18

TABLE 1.

Studies using specifically named defined communities to study host-microbe interactions in vivo (n = 31)a

Consortium (no. of speciesb) Division of phylae Strain source(s) Host species (strain) Part of the gut studiedf No. of animals/group Chow Sex Age (collection time[s]c) Study outcome(s)d Reference
Schaedler flora (5 species)
 2 Lactobacillus spp., anaerobic Streptococcus sp. (group N), Bacteroides strain, Enterococcus sp., coliform strain
graphic file with name MMBR.00054-18-f0124.jpg Mouse Mouse (NR) graphic file with name MMBR.00054-18-f0026.jpg 20 NR NR 4 wk (3 wk–4 mo) Colonization pattern; cecal size 9
ASF (8 species)
 ASF356: Clostridium species
 ASF360: Lactobacillus intestinalis or Lactobacillus acidophilus
 ASF361: Lactobacillus murinus or Lactobacillus salivarius
 ASF457: Mucispirillum schaedleri
 ASF492: Eubacterium plexicaudatum
 ASF500: Pseudoflavonifractor sp.
 ASF502: Clostridium sp.
 ASF519: Parabacteroides distasonis
graphic file with name MMBR.00054-18-f0125.jpg Mouse Mouse (HA/ICR) graphic file with name MMBR.00054-18-f0027.jpg 30 NR Both Adult (14–56 days) Death after C. botulinum infection; fecal C. botulinum toxin excretion; colonization pattern of C. botulinum 36
Mouse Rat (F344) graphic file with name MMBR.00054-18-f0028.jpg 1–5 Sterile food (Charles River) ad libitum M NR (2 wk) Hepatic genotoxicity of mononitrotoluene isomers; metabolic activation of 2NT by intestinal bacteria; cecal bacterial content 169
Mouse Mouse (scid C.B-17) graphic file with name MMBR.00054-18-f0029.jpg 4–6 Autoclaved pelleted diet ad libitum NR NR (8–12 wk postreconstitution CD4+ T cells) After Helicobacter hepaticus infection, rectal prolapse; clinically severe disease; grossly thickened colon, cecum, and rectum on necropsy; colonic inflammation score; colonic epithelial cell proliferation; histopathology 16
Mouse Rat (HLA-B27 on 33-3/F344) graphic file with name MMBR.00054-18-f0030.jpg 7–11 NR At least M 2 mo (1 mo) Gross gut score, levels of MPO and IL-1B in cecal tissue; histological inflammatory score of cecum and antrum 15
Mouse Mouse (C3H/HeN) graphic file with name MMBR.00054-18-f0031.jpg 4–8 Irradiated diet (Harlan Teklad) NR 6–8 wk (9–14 wk) After colonization with Helicobacter bilis or Brachyspira hyodysenteriae, cecal pathological gross and histological scores; serum IgG1 + IgG2a Ab response 170
Mouse Mouse (C3H/HeN) graphic file with name MMBR.00054-18-f0032.jpg 7–10 Irradiated diet (Harlan Teklad) NR 6–8 wk (10 wk) Fecal bacterial contents (after H. bilis infection); cecal pathological scores; cecal histological changes; serum immunoglobulin 171
Mouse Mouse (SW) graphic file with name MMBR.00054-18-f0033.jpg 2–5 NR NR 6–9 wk (NR) Presence of Th17 cells and Foxp3+ regulatory cells in LP of small intestine 172
Mouse Mouse (C57BL/6) graphic file with name MMBR.00054-18-f0034.jpg NR NR NR NR Total intestinal IgA and intestinal IgA, anti-CBir1; proliferation of splenic CBir1 TgT cells after CBir1 gavage 173
Mouse Mouse(B6.Rag−/−) graphic file with name MMBR.00054-18-f0035.jpg NR NR F 8–10 wk (10 days) Homeostatic and spontaneous proliferation of TCR TgT cells in LP 174
Mouse Mouse (C57BL/6) graphic file with name MMBR.00054-18-f0036.jpg 5–8 Autoclaved chow NR 8 wk (at least 3 dpi) After infection, S. Typhimurium levels in mesenteric lymph nodes, spleen, cecum, and feces; cecal pathology score; cecal microbiota density; bacterial content and microbiota complexity in feces 97
ASF (8 and 9 species)
 8 species: ASF
 9 species: ASF + Escherichia coli HA108 or HA107
9 species:
Inline graphic
Mouse Mouse(C57BL/6) graphic file with name MMBR.00054-18-f0037.jpg 3 NR NR NR (119 days) No. of IgA plasma cells per intestinal villus in duodenum, jejunum, ileum, and colon; IgA-bacterium binding in intestine; anti-E. coli IgA titer 21
ASF (8 species) Mouse Mouse (NMRI, C57BL/6, BALB/c, NIH Swiss, SW, NMRI, MyD88−/− Ticam1−/−, SMARTA, C57BL/6.CD45.1+) graphic file with name MMBR.00054-18-f0038.jpg 3–10 NR NR NR (up to 28 days) Cecal bacterial contents; colonic Treg cell response and relative IL-10 expression in spleen, MLN, Peyer’s patches, colonic and small intestinal LP, thoracic duct lymph; IL-17 production; relative abundance of strains; microscopic localization in colon and small intestine 175
Mouse Mouse (Nod1−/− and Nod2−/− on C57BL/6 background) graphic file with name MMBR.00054-18-f0039.jpg NR NR NR 6–9 wk (NR) Cecal bacterial contents; intestinal tissue conductance and Cr-EDTA flux; E-cadherin protein expression and RegIII-gamma mRNA expression in colon; survival, colitis disease severity, histology score, and myeloperoxidase activity after DSS induction; colonic IL-6, IL-10, MCP-1, IFN-c, TNF-α, IL-12p70 levels 17
Mouse Mouse (C57BL/6) graphic file with name MMBR.00054-18-f0040.jpg NR Autoclaved food Both 8–12 wk (8–12 wk) RegIII-gamma RNA and protein expression in ileum and colon 176
Mouse Mouse (C57BL/6 and C57BL/6 TSLPR−/−) graphic file with name MMBR.00054-18-f0041.jpg 3–5 NR NR NR (28 days) Expression of thymic stromal lymphopoietin mRNA in intestinal epithelial cell or colonic LP (LP); % of CD4+ T cells secreting IL-17A and IFN gamma in the colonic LP and MLN; expansion of colonic Treg cells in colonic LP and MLN; expression of receptor for TSLP by CD4+ and regulatory T cells 177
Mouse Mouse (NIH Swiss) graphic file with name MMBR.00054-18-f0042.jpg 4 NR NR 3 days (3 days) Structure of myenteric plexus, nerve density, average no. of HuC/D-positive myenteric neurons per ganglion, cell body size, and average no. of nNOS-positive neurons per myenteric ganglion in duodenum, jejunum, and ileum; small intestinal motility (frequency and amplitude of muscle contractions) in duodenum, jejunum, and ileum before and after general neural or specific nitrergic blockade 178
Mouse Mouse (C57BL/6) graphic file with name MMBR.00054-18-f0043.jpg 5–14 Autoclaved mouse breeder’s diet (Harlan), unlimited access Both 6–12 wk (3 wk) Colonic histology, inflammatory (MPO) activity, enteropathy (presence of fecal albumin), and cytokine expression; fecal microbiota profiles; colonic gene expression; proportion of T-cell subtypes in colonic LP and other mucosal and systemic immune compartments 81
ASF (8 species) (Oligo-MM12 was also used, but no host parameters were assessed) Mouse Mouse (C57BL/6) graphic file with name MMBR.00054-18-f0044.jpg 3 (ASF), 5–23 (Oligo-MM) NR Both NR Thicknesses of total colon and colon inner mucus (ASF); mucus turnover time (ASF); alpha diversity in colon and cecum (Oligo-MM) 26
ASF (8 and 9 species)
 8 species: ASF
 9 species: ASF + Oxalobacter formigenes
9 species:
Inline graphic
Mouse Mouse (SW) graphic file with name MMBR.00054-18-f0045.jpg 4–7 LM-485 autoclavable rodent diet, free access M (no gender effect observed) 3–9 mo (3–9 mo + 6 wk) Bacterial levels in stomach, cecum, proximal colon, and cecal mucosa; body wt; dietary oxalate intake; cecal and fecal oxalate levels; urine vol; urinary metabolite levels; cecal wet wt; cecal water metabolites 20
Partial ASF (6 species)
 ASF356, -361, -492, -502, -519, and -500 (ASF360 and -457 did not colonize)
graphic file with name MMBR.00054-18-f0007.jpg Mouse Mouse (NOD.MyD88KO) None 9–23 NR Both NR (up to 30 wk) Incidence of diabetes; histological scores of pancreatic islet destruction 18
Partial ASF (4 and 5 species)
 4 species: ASF360, ASF361, ASF457, ASF519
 5 species: 4 species + Butyrivibrio fibrisolvens (type I, ATCC 19171; type II, ATCC 51255)
4 species:
Inline graphic
5 species:
Inline graphic
Mouse and bovine Mouse (BALB/c) graphic file with name MMBR.00054-18-f0046.jpg 4–5 Autoclaved low-fiber diet (5SRZ, catalog no. 1813680), high-fiber diet (5SVL, catalog no. 1813901), or tributyrin diet (5AVC, catalog no. 1814961) NR NR (2.5–5 mo after colorectal cancer induction) Colorectal tumor multiplicity, tumor size, and tumor grade; levels of LDHA, lactate, butyrate, H3ac, and total H3 in colonic tissue and tumors; luminal SCFA levels; H3ac and expression levels of Fas, p21, and p27 genes in colonic tissue and tumors; apoptosis and cell proliferation levels in colonic tissue and tumors 19
Partial ASF (4, 5, 7, and 7 species)
 4 species: ASF356, ASF360, ASF361, and ASF519
 5 species: ASF360, ASF361, ASF457, SB2 (ASF502), and ASF519
 7 species: ASF356, ASF360, ASF361, ASF457, ASF500, SB2 (ASF502), and ASF519
 7 species: 4 species + E. coli Mt1B1, Streptococcus danieliae ERD01G, Staphylococcus xylosus 33-ERD13C (more with Oligo-MM [see below])
4 species:
Inline graphic
5 species:
Inline graphic
7 species:
Inline graphic
7 species:
Inline graphic
Mouse Mouse (C57BL/6) graphic file with name MMBR.00054-18-f0047.jpg 4–6 NR Both 0 or 8–12 wk (8–12 wk or 40 days) Fecal bacterial content; bacterial load of S. Typhimurium in feces, cecum, and MLN; relative cecal wt; functional genomic analysis of bacteria 22
Oligo-MM (12, 15, and 17 species)
 12 species, Oligo-MM: Acutalibacter muris KB18, Flavonifractor plautii YL31, Clostridium clostridioforme YL32, Blautia coccoides YL58, Clostridium innocuum I46, Lactobacillus reuteri I49, Enterococcus faecalis KB1, Bacteroides caecimuris I48, Muribaculum intestinale YL27, Bifidobacterium longum subsp. animalis YL2, Turicimonas muris YL45, Akkermansia muciniphila YL44
 15 species: 12 species + 3 facultative anaerobes (E. coli Mt1B1, Streptococcus danieliae ERD01G, Staphylococcus xylosus 33-ERD13C)
 17 species: 12 species + 5 ASF members (ASF360, ASF361, ASF457, SB2 [ASF502], ASF519)
12 species:
Inline graphic
15 species:
Inline graphic
17 species:
Inline graphic
Mouse Mouse (C57BL/6) graphic file with name MMBR.00054-18-f0048.jpg 4–6 NR Both 0 (8–12 wk) Fecal bacterial content; bacterial load of S. Typhimurium in feces, cecum, and MLN; relative cecal wt; functional genomic analysis of bacteria 22
Oligo-MM (12 and 13 species)
 12 species: Oligo-MM
 13 species: 12 species + Clostridium scindens ATCC 35704
12 species:
Inline graphic
13 species:
Inline graphic
Mouse Mouse (C57BL/6) graphic file with name MMBR.00054-18-f0049.jpg 5–8 NR NR 0 (6–12 wk) Fecal and cecal bacterial contents; cecal levels of lipocalin-2; calprotectin expression in cecal tissue; histopathology of cecum; cecal bile acid metabolome
SIHUMI(x) (7 and 8 species):
 SIHUMI: Anaerostipes caccae DSM 14662 or DSM 14667, Bacteroides thetaiotaomicron DSM 2079, B. longum NCC 2705, Blautia producta DSM 2950, Clostridium ramosum DSM 1402, E. coli K-12 MG1655, Lactobacillus plantarum DSM 20174
 SIHUMI(x) Clostridium butyricum DSM 10702
7 species:
Inline graphic
8 species:
Inline graphic
Human Rat (Sprague-Dawley) graphic file with name MMBR.00054-18-f0050.jpg 3–21 Sterilized standard chow (225 g/kg of body wt protein, 50 g/kg crude fat, 65 g/kg ash, 135 g/kg moisture, 480 g/kg N-free extract), fermentable-fiber-free diet, inulin diet, pectin diet, and high-fat and low-fat diets Both 0–3 mo (2–38 wk) Stability of microbiota in offspring; SCFA concn and pH in cecum, colon, and feces; bacterial counts in cecum, colon, and feces; Midtvedt criteria 27
SIHUMI(x) (8 and 9 species)
 8 species: SIHUMI(x)
 9 species: 8 species + A. muciniphila ATCC BAA-835
9 species:
Inline graphic
Human Mouse (C3H) graphic file with name MMBR.00054-18-f0051.jpg 5–10 NR NR 12 wk (5–15 days) Bacterial cell no. and proportions in cecum and colon; cecal and colonic histopathology scores; expression of proinflammatory cytokines in cecal and colonic mucosa; serum protein levels of proinflammatory cytokines; no. of S. Typhimurium cells in MLN and spleen; size; macrophage infiltration in cecal tissue; localization of A. muciniphila and S. Typhimurium; mucin formation, mucus thickness, mucus composition, and no. of mucin-filled cells 28
SIHUMI(x) (8 and 9 species)
 8 species: SIHUMI(x)
 9 species: 8 species + Fusobacterium varium ATCC 8501
9 species:
Inline graphic
Human Mouse (C3H/HeOuJ) graphic file with name MMBR.00054-18-f0052.jpg 12 Irradiated standard chow R03-40 F 0 (8 wk) Body wt; dry mass of cecum and colon; bacterial content in cecum and colon; polyamine concn in cecum and colon; SCFA concn in cecum and colon; histology of cecum and distal colon (thicknesses of crypt, epithelial layer, mucosa, submucosa, muscularis externa); mitosis and apoptosis of cecal and distal colonic tissue 30
Human Mouse (Prm/Alf, C3H/He) graphic file with name MMBR.00054-18-f0053.jpg 12–13 Sterilized pelleted standard chow R03-40 F 0 (56 ± 1 days) Lengths of small, large, and whole intestines; thicknesses of muscle, crypt, and villi in proximal and small intestine and colon; fecal and cecal microbial contents; cecal concn of SCFAs and polyamines 31
SIHUMI(x) (7 and 8 species)
 7 species: SIHUMI(x) without C. ramosum
 8 species: SIHUMI(x)
7 species:
Inline graphic
8 species:
Inline graphic
Human Mouse (C3H/HeOuJ) graphic file with name MMBR.00054-18-f0054.jpg 3–9 Irradiated low-fat or high-fat diet ad libitum M 0 (16 wk) Body wt; % body fat; adipose tissue wt (epididymal, mesenteric, and subcutaneous); energy intake; food efficiency; digestibility of high-fat diet; digestible energy; cecal and colonic bacterial contents per species; blood glucose; leptin gene expression in epididymal tissue; liver wt; liver triglyceride levels; liver glycogen contents; expression of genes involved in lipid transport, lipid synthesis, cholesterol synthesis, and lipid catabolism; gene expression of proteins involved in small intestinal glucose uptake; SCFA formation in cecum, colon, and portal vein plasma; gene expression of SCFA-related proteins in colonic mucosa; gene expression of lipid transport and storage proteins in ileum; parameters of intestinal permeability and low-grade inflammation 32
SIHUMI(x) (8 and 9 species)
 8 species: SIHUMI(x)
 9 species: 8 species + A. muciniphila ATCC BAA-835
9 species:
Inline graphic
Human Mouse (C57BL/6.129P2-Il10tm1Cgn) graphic file with name MMBR.00054-18-f0055.jpg 5–6 Irradiated standard chow (fortified type 1310; Altromin, Lage, Germany) ad libitum M 0 or 8 wk (3 wk) Body wt; histopathology scores in submucosa, LP, surface epithelium, and lumen; colon length; relative mRNA levels of Tnfa, Ifng, and Reg3g; fecal lipocalin-2 concn; fecal and cecal bacterial levels; cecal histology; no. of goblet cells per 100 epithelial cells in cecum and colon; mucus layer thickness in colon; relative Muc2 mRNA levels in distal small intestine, cecum, and colon 29
a

Abbreviations: M, male; F, female; SW, Swiss Webster; LP, lamina propria; MLN, mesenteric lymph nodes; MPO, myeloperoxidase; NR, not reported; SCFA, short-chain fatty acid; Treg cell, regulatory T cell; IL-1B, interleukin-1B; Ab, antibody; TCR, T-cell receptor; dpi, days postinfection; DSS, dextran sodium sulfate; IFN, interferon; TNF-α, tumor necrosis factor alpha; 2NT, 2-nitrotoluene; H3ac, pan-histone 3 acetylation; LDHA, lactate dehydrogenase A; nNOS, neuronal nitric oxide synthase; TgT cells, transgenic T cells; MCP-1, monocyte chemoattractant protein 1.

b

Two different strains tested are counted as one species. Strains were not always reported. Pathogenic species, in the case of an infection model, are not included.

c

The colonization time includes the time from colonization (time zero in the case of transfer of microbiota to offspring) until and including the time of sacrifice or the end of experimental (e.g., dietary) manipulations, in cases where this is clearly stated in the paper. If age is given and animals are colonized at birth, the age is included in the colonization time.

d

Study outcomes are reported only for animals colonized with the defined community of interest.

e

Inline graphic, Firmicutes; Inline graphic, Bacteroidetes; Inline graphic, Actinobacteria; Inline graphic, Proteobacteria; Inline graphic, Verrucomicrobia; Inline graphic, other.

f

The color codes from left to right in the illustration are as follows: Inline graphic, stomach; Inline graphic, duodenum; Inline graphic, jejunum; Inline graphic, ileum; Inline graphic, cecum; Inline graphic, colon; Inline graphic, rectum; Inline graphic, feces.