Using In Vitro Models to Study the Interactions Between Environmental Exposures and Human Microbiota
Abstract
1. Introduction
2. Methods
2.1. Search Strategy
2.2. Eligibility Criteria
2.3. Data Extraction and Synthesis
3. Results
3.1. Gastrointestinal Tract Microbiota
3.1.1. Oral Microbiota
3.1.2. Gastric and Small Intestinal Microbiota
Exposure | In Vitro Model | Key Findings 1 | Methodology 3 | Reference |
---|---|---|---|---|
Oral cavity microbiota | ||||
| Six-species biofilm on sintered hydroxyapatite disks | Total bacteria (-) | Viable cell counting | [54] |
| Saliva-derived mixed-species biofilm on saliva-coated human enamel discs | Streptococcus mutans (↓) Streptococcus sanguinis (↓) | qPCR | [44] |
| Saliva-derived mixed-species culture | Uncultured Veillonella sp. (↑) Bulleidia extructa (↑) Veillonella atypica and three Veillonella sp. (↓) | DGGE | [48] |
| Saliva-derived mixed-species biofilm on saliva-coated human enamel discs | Streptococcus mutans (↓) Streptococcus sanguinis (↑) | qPCR | [44] |
| Oral isolate single-species culture | Enterobacter hormaechei (↓) Streptococcus salivarius (↓) Staphylococcus aureus (↓) Enterobacter cloacae (↓) Enterococcus faecalis (↓) Lactobacillus salivarius (↓) Candida albicans (↓) | Viable cell counting | [51] |
| Saliva-derived mixed-species biofilm in hydroxyapatite disc reactors | Total facultative anaerobes (↓) Total anaerobes (-) Total streptococci (-) Total Gram-negative anaerobes (↓) | Viable cell counting | [42] |
| Saliva-derived mixed-species biofilm in drip-flow biofilm reactors | Total facultative anaerobes (↓) Total anaerobes (↓) Total streptococci (↓) Total Gram-negative anaerobes (↓) | Viable cell counting | [42] |
| Saliva-derived mixed-species biofilm in multiple sorbarod devices | Total facultative anaerobes (-) Total anaerobes (-) Total streptococci (-) Total Gram-negative anaerobes (↓) | Viable cell counting | [42] |
| Saliva-derived mixed-species biofilm in hydroxyapatite disc reactors | Total facultative anaerobes (↓) Total anaerobes (↓) Total streptococci (↓) Total Gram-negative anaerobes (↓) | Viable cell counting | [42] |
| Saliva-derived mixed-species biofilm in drip-flow biofilm reactors | Total facultative anaerobes (↓) Total anaerobes (↓) Total streptococci (↓) Total Gram-negative anaerobes (↓) | Viable cell counting | [42] |
| Saliva-derived mixed-species biofilm in multiple sorbarod devices | Total facultative anaerobes (-) Total anaerobes (-) Total streptococci (↓) Total Gram-negative anaerobes (↓) | Viable cell counting | [42] |
| Oral cavity-derived isolate single-species culture | Enterobacter hormaechei (↓) Streptococcus salivarius (-) Staphylococcus aureus (↓) Enterobacter cloacae (-) Enterococcus faecalis (↓) Lactobacillus salivarius (-) Candida albicans (↓) | Viable cell counting | [51] |
| Single-species culture and biofilm in culture plates; dual-species culture and biofilm in culture plates | Streptococcus mutans (↓) Candida albicans (↓) Staphylococcus aureus (↓) Pseudomonas aeruginosa (↓) | Viable cell counting | [57] |
| Oral cavity-derived Candida albicans isolate single-species culture | Candida albicans (↓) | Cell counting, optical density measurement | [56] |
| Mixed-species biofilm in culture plates, and plates supplemented with nylon fibers | Mixtures of 5–6 species selected from Actinomyces viscosus, Enterococcus faecalis, Streptococcus mutans, Streptococcus oralis, Streptococcus sanguinis, and Streptococcus salivarius (↓) | Visual turbidity, viable cell counting, crystal violet staining | [52] |
| Single-species culture on agar plates | Porphyromonas gingivalis (↓) Prevotella intermedia (↓) Fusobacterium nucleatum (↓) Staphylococcus aureus (↓) Streptococcus mutans (↓) | Agar well diffusion assay | [58] |
| Single-species culture on agar plates | Streptococcus mutans (↓) Streptococcus sanguinis (↓) Staphylococcus aureus (↓) Candida albicans (↓) | Disc diffusion assay | [59] |
| Saliva-derived mixed-species culture | Porphyromonas pasteri (↓) | 16S rRNA gene sequencing | [49] |
| Nine-species biofilm on polymethylmethacrylate discs | Total aerobes (↓) Total anaerobes (↓) Candida (↓) | qPCR | [60] |
| Teeth crown surface-derived mixed-species culture | Total bacterial counts (↓) | Viable cell counting | [41] |
| Saliva-derived mixed-species biofilm in Constant Depth Film Fermenters | Total anaerobic count (↓) Lactobacillus (-) Streptococcus (↓) Actinomyces (↓) | Viable cell counting | [43] |
| Saliva-derived mixed-species biofilm in culture plates pre-coated with saliva pellicle | Veillonella atypica (↑) Veillonella infantium (↑) Veillonella dispar (↑) Veillonella parvula (↓) Prevotella jejuni (↑) Prevotella histicola (↑) Prevotella salivae (↑) Prevotella melaninogenica (↑) Streptococcus oralis (↓) Streptococcus mitis (↓) Streptococcus parasanguinis (↓) Streptococcus sanguinis (↓) Streptococcus salivarius (↑) Streptococcus pneumoniae (-) Staphylococcus aureus (-) | Metagenomic shotgun sequencing | [45] |
| Saliva-derived mixed-species biofilm in culture plates | Total viable cells (-) Streptococcus salivarius (↑) Streptococcus pneumoniae (↑) Lactobacillus fermentum (↓) | Viable cell counting, metagenomic shotgun sequencing | [46] |
| Mixed-species biofilm in sintered hydroxyapatite disc reactors | Fusobacterium nucleatum was associated with carbohydrate metabolism (↑), cofactors, vitamins, prosthetic groups and pigments (↑), amino acid metabolism (↑), virulence mechanisms (↑), respiration (↓) | Metatranscriptomic sequencing | [53] |
| Single-species biofilm in culture plates | Streptococcus mutans biofilm (↑) | Crystal violet staining | [61] |
| Mixed-species biofilm on sintered hydroxyapatite disks, with or without organoid tissue overlay | Without overlay: quorum-sensing regulated gene expression (↑), biofilm surface area (↑) With overlay: keratin thickness (↑), host response to pathogen-rich biofilms (↓) | NMR spectroscopy, TIMS-TOF, CLSM | [55] |
| Saliva-derived mixed species culture in 3D oral mucosa models | Alpha diversity (↑) Clostridium (↑) Prevotella (↑) Veillonellaceae (↑) Bacteroides (↑) Multiple glucose and energy metabolic pathways (↑) | 16S rRNA gene sequecning, GC-MS | [62] |
| Single-species culture and biofilm in culture plates; dual-species biofilm on glass coverslips pre-coated with saliva; saliva-derived mixed-species biofilm on glass coverslips pre-coated with saliva | Streptococcus sanguinis (↓) Streptococcus mutans (↓) Streptococcus mutans/Streptococcus sanguinis ratio (↓) | Optical density meansurement, FISH, EPS staining | [50] |
| Candida albicans, Candida glabrata, Streptococcus salivarius, and Klebsiella oxytoca single-species culture and biofilm in culture plates | Planktonic cell growth (-) Klebsiella oxytoca and Candida glabrata biofilms exhibited varying responses to different culture conditions | Optical density meansurement, crystal violet staining, calcofluor white staining | [63] |
| Single-, dual-, and saliva-derived mixed-species culture | Streptococcus (↑) Streptococcus mutans/Streptococcus sanguinis ratio (↑) | Viable cell counting, qPCR, FISH, MTT assay, crystal violet staining, EPS staining, RNA sequencing | [47] |
| Porphyromonas gingivalis, Actinobacillus actinomycetemcomitans, Actinomyces odontilyticus single-species culture supernatant, co-cultured with ACE2 + 293 T cells | SARS-CoV-2 pseudoviral infection (↓) | Luciferase activity measurement | [64] |
| Streptococcus sanguinis and Akata cell co-culture | EBV lytic activation (↑) | Flow cytometry, qPCR | [65] |
Gastric microbiota | ||||
| Eleven-species culture in chemostats | Candida (-) Lactobacillus (-) Escherichia (↓) Klebsiella (↓) | Viable cell counting | [66] |
Small intestinal microbiota | ||||
| Seven-species culture in the Smallest Intestine (TSI) model inoculated with Listeria monocytogenes | Streptococcus (-) Enterococcus faecalis (-) Listeria monocytogenes (↓) Escherichia coli (-) | Viable cell counting | [75] |
| Seven-species culture in the Smallest Intestine (TSI) model inoculated with Listeria monocytogenes | Streptococcus (-) Enterococcus faecalis (↓) Listeria monocytogenes (-) Escherichia coli (↓) | Viable cell counting | [75] |
Large intestinal microbiota 2 | ||||
| [24,25,26,33] | |||
| ||||
| [8,9] | |||
| [10,11] | |||
| [34,35] | |||
| [12,13] | |||
| [36,37] | |||
| [20,38] |
3.2. Extraintestinal Microbiota
3.2.1. Respiratory Microbiota
3.2.2. Skin Microbiota
3.2.3. Vaginal Microbiota
Exposure | In Vitro Model | Key Findings 1 | Methodology 2 | Reference |
---|---|---|---|---|
Respiratory tract microbiota | ||||
| Nose-derived Staphylococcus isolates on agar plates | 87 out of 88 fluoroquinolone- resistant staphylococci carried co-resistance, and 75 carried co-resistance specifically to meticillin | Disc diffusion assay | [78] |
| Nose-derived Staphylococcus isolates on agar plates | 24 out of 27 Staphylococcus carried resistance to penicillin and/or cefoxitin | Viable cell counting | [83] |
| Throat- and nose-derived Haemophilus parainfluenzae isolates on agar plates | Isolates showed different resistance patterns based on two different guidelines | Disc diffusion assay | [84] |
| Respiratory tract-derived Prevotella isolates on agar plates | 38 out of 50 Prevotella isolates produced extended-spectrum β-lactamases and had higher resistance to amoxicillin and ceftazidime | Disc diffusion assay, Etest | [79] |
| Nose-derived single-species isolates on agar plates | 6 out of 8 Moraxella catarrhalis isolates carried resistance to amoxicillin and TMP/SMX, 2 of these 6 exhibited ceftriaxone resistance, and 1 exhibited azithromycin resistance 12 our of 45 Streptococcus pneumoniae isolates demonstrated azithromycin resistance, and 14 showed resistance to TMP/SMX | Etest | [85] |
| Sputum-derived mixed-species culture | Candida albicans (↓) Aspergillus fumigatus (↓) Actinomyces oris (↓) Schaalia odontolytica (↓) Rothia mucilaginosa (↓) Multiple Streptococcus species (↓) Pseudomonas aeruginosa (-) Staphylococcus aureus (-) | Metagenomic shotgun sequencing | [86] |
| Corynebacterium, Haemophilus influenzae, Calu-3 cell co-culture in the air-liquid interface (ALI) model | HRV copy number (↓) by Corynebacterium pseudodiphtheriticum + Haemophilus influenzae | qRT-PCR | [77] |
Skin microbiota | ||||
| Staphylococcus epidermidis single-species culture | Yields of short-chain fatty acids depended on different cosmetics | HPLC | [89] |
| Lactobacillus crispatus, Staphylococcus epidermidis, and Cutibacterium acnes single-species culture in a culture plate exposed to UV light | Lactobacillus crispatus (↑) Cutibacterium acnes (↓) | Viable cell counting | [90] |
| Skin-derived single-species culture | Deinococcus grandis and Stenotrophomonas grew by metabolizing octocrylene | Optical density measurement | [91] |
| Sphingomonas mucosissima single-species culture on agar plates | Sphingomonas mucosissima was resistant to UVR at both wavelengths | Visual observation | [92] |
| Skin-derived Staphylococcus aureus, Staphylococcus epidermidis, Staphylococcus hominis, Micrococcus luteus, Corynebacterium stearicum, and Moraxella osloensis single-species culture | UVA: complete inhibition of all microorganisms UVB: strain-dependent inhibition Combination: similar to UVA | Optical density measurement | [93] |
| Cutibacterium acnes and Lactobacillus fermentum single-species culture | Both microorganisms (↓) | Viable cell counting | [94] |
| Skin-derived single-species fungal spores on agar plates | Aspergillus flavus (↑) Aspergillus niger (↑) Penicillium rubens (↓) | Germinated spore quantification | [95] |
| Skin-derived Micrococcus luteus and Pseudomonas oleovorans co-culture in a microbially competent 3D skin model | Benzo[a]pyrene degradation to various metabolites | GC-MS | [87] |
| Single-species culture | Staphylococcus, Corynebacterium, Micrococcus, Dermacoccus, and Kocuria species metabolized Methyl Red with various rates, and all but Corynebacterium xerosis metabolized Orange II | Spectrophotometry | [96] |
| Staphylococcus epidermidis single-species culture on agar plates | Staphylococcus epidermidis exhibited resistance to various antibiotics, and antibiotic-adapted strains showed cross-resistance | Disc diffusion assay | [97] |
| Single-species culture on agar plates | Micrococcus luteus (↓) Staphylococcus epidermidis (↓) Clostridium xerosis (↓) Bacillus subtilis (↓) | Optical density measurement | [98] |
Vaginal microbiota | ||||
| Vagina-derived single species or mixed species co-cultured with vaginal epithelial cells and HIV-1-susceptible cells in the air-liquid interface (ALI) model | HIV-1 replication (↓) by Lactobacillus iners and group B streptococcus-dominated culture | qRT-PCR | [102] |
| Vagina-derived single species or mixed species co-cultured with vaginal epithelial cells in the air-liquid interface (ALI) model | ZIKV titers (↓) by Staphylococcus epidermidis-dominated culture ZIKV titers (↑) by Lactobacillus crispatus-dominated culture HSV- HSV-2 (↑) by Lactobacillus jensenii-dominated, Mobiluncus mulieris-containing culture | qPCR | [105] |
| Lactobacillus single-species culture on agar plates | Pathogens (↓) by Lactobacillus species except for L. iners, with strain-specific differences | Zone of inhibition surrounding Lactobacillus | [106] |
| Vagina-derived Lactobacillus single-species culture on agar plates | Pathogens (↓), with strain-specific differences | Spots-on-lawn test | [107] |
| Streptococcus agalactiae and Lactobacillus iners single-species culture | Lactobacillus iners (↓) upon TV exposure, and (-) six hours later Streptococcus agalactiae (↑) | Viable cell counting | [108] |
| Vagina-derived Lacticaseibacillus rhamnosus single-species culture | Mycobacterium tuberculosis (↓) | Viable cell counting | [109] |
| Vagina-derived mixed-species culture on agar plates | Gardnerella (↓) | Zone of inhibition surrounding mixed-species culture | [110] |
| Lactobacillus crispatus, Lactobacillus iners, Gardnerella vaginalis, Prevotella bivia, and Atopobium vaginae co-culture | Gardnerella vaginalis (↓) Prevotella bivia (↓) Atopobium vaginae (↓) Lactobacillus crispatus (-) Lactobacillus iners (-) | Optical density measurement | [103] |
| Gardnerella vaginalis and Lactobacillus iners co-culture | Gardnerella vaginalis (-) due to metronidazole sequestration by Lactobacillus iners | Viable cell counting | [99] |
| Vagina-derived Bifidobacterium single-species culture on agar plates | Bifidobacterium exhibited different susceptibility to metronidazole and clindamycin, with species-specific patterns | Etest | [104] |
| Vagina-derived Lactobacillus single-species culture on agar plates | Lactobacillus showed species- and strain-dependent antibiotic resistance patterns | Disc diffusion assay | [107] |
| Gardnerella vaginalis single-species culture | Gardnerella vaginalis showed strain-dependent antibiotic resistance patterns | Optical density measurement | [111] |
| Vagina-derived single-species culture | Candida (↓) at low oil concentration Bifidobacterium (↓) at intermediate concentration Lactobacillus (↓) at high concentration | Agar well diffusion assay | [112] |
| Lactobacillus single-species culture | Lactobacillus (↓) | Minimal inhibiting concentration measurement | [113] |
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
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Cheng, Q.; Chen, S. Using In Vitro Models to Study the Interactions Between Environmental Exposures and Human Microbiota. Microorganisms 2025, 13, 247. https://doi.org/10.3390/microorganisms13020247
Cheng Q, Chen S. Using In Vitro Models to Study the Interactions Between Environmental Exposures and Human Microbiota. Microorganisms. 2025; 13(2):247. https://doi.org/10.3390/microorganisms13020247
Chicago/Turabian StyleCheng, Qiwen, and Shengxi Chen. 2025. "Using In Vitro Models to Study the Interactions Between Environmental Exposures and Human Microbiota" Microorganisms 13, no. 2: 247. https://doi.org/10.3390/microorganisms13020247
APA StyleCheng, Q., & Chen, S. (2025). Using In Vitro Models to Study the Interactions Between Environmental Exposures and Human Microbiota. Microorganisms, 13(2), 247. https://doi.org/10.3390/microorganisms13020247