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