Residents or Tourists: Is the Lactating Mammary Gland Colonized by Residential Microbiota?
Abstract
:1. Introduction
2. Conceptualizing a Residential Mammary Microbiome
3. Evidence That the Human Milk Microbiota Are “Tourists”
3.1. There Is a Constant Low-Grade Influx of Bacteria from other Sources
3.1.1. Infant Oral Cavity
3.1.2. Maternal Skin
3.1.3. Maternal Gut
3.2. Human Milk Is a Hostile Environment for Bacteria
3.2.1. Secretory Immunoglobulin A
3.2.2. Human Milk Oligosaccharides
3.2.3. Lysozyme and Lactoferrin
3.2.4. Immune Cells
4. Evidence That the Human Milk Microbiota Are “Residents”
4.1. Human Milk Is a Nutrient-Rich Environment
4.2. Biofilm Formation
4.2.1. Staphylococcus Species
4.2.2. Streptococcus Species
4.2.3. Enterococcus Species
4.2.4. Lactic Acid Bacteria
Biofilm-Forming Bacteria | Reference | Origins of Tested Isolates | Number of Tested Strains | Biofilm Testing Method | Biofilm Genes or Proteins Identified | Study Findings | |
---|---|---|---|---|---|---|---|
Staphylococcus species | S. aureus and coagulase-negative Staphylococcus | Darwish and Asfour 2013 [72] | Bovine mastitis milk samples | 108 (40 S. aureus and 68 coagulase-negative Staphylococcus isolates) | Congo Red Agar method; microtiter plate method | Genes eno, icaA, icaD, and bap | By the Congo Red Agar method, 67.5% of S. aureus and 72.1% of coagulase-negative Staphylococci were biofilm producers; by the microtiter plate method, 100% of S. aureus and 94.1% of coagulase-negative Staphylococci were biofilm producers. |
Coagulase-negative Staphylococcus including S. chromogenes, S. simulans, and S. epidermidis | Simojoki et al., 2012 [73] | Bovine mastitis milk samples | 244 isolates | Tissue culture plate assay and fluorescent in situ hybridization | Genes encoding the adhesion proteins MSCRAMM, as well as biofilm-associated proteins eno and bap | A total of 40% of tested S. epidermidis isolates produced slime. | |
Streptococcus species | S. mitis | Rørvik et al., 2021 [77] | Mutants generated by markerless gene editing | 8 strains | 0.1% Safranin staining and quantification | Genes cdaA, pde1, and pde2 | S. mitis biofilm formation was associated with gene cdaA, pde1, and pde2. |
S. parasanguinis | Chen et al., 2020 [88] | Type cultures | 6 strains | Biofilm structure was examined by confocal laser scanning microscopy | Protein Fap1, BapA1, and FimA | S. parasanguinis biofilm formation was associated with collagen-binding proteins. | |
S. mitis | Harth-Chu et al., 2019 [78] | Oral mucosal sites of healthy infants; oral cavity, dental biofilms, or bloodstream of patients with clinical symptoms of bacteremia or septicemia | 20 strains | Microtiter plate method | Genes pcsB | S. mitis biofilm formation was associated with gene pcsB. | |
S. anginosus | Perez-Tanoira et al., 2019 [82] | Salivary stones from patients with sialolithiasis | 10 isolates | Fluorescence microscopy and sonication | ·· | S. anginosus had the ability to form biofilms in the human oral cavity. | |
S. salivarius | Couvigny et al., 2018 [75] | Wild-type strains and mutants, clinical isolates from human blood, oral cavity, human milk, sputum, peritoneal cavity, trachea, and lower-left lung | 28 isolates | Confocal laser scanning microscopy | Gene bglB, cshA, gtfH, liaR, asp1, asp2, cwpB, cwpK, gtfE, gtfG, secA2, and srtA | S. salivarius had the ability to auto-aggregate and form biofilms. | |
S. parasanguinis | Liang et al., 2011 [81] | Type cultures | 7 strains | Microtiter plate method and plastic coverslip method | Cell surface protein BapA1 | Protein BapA1 contributed to the biofilm formation of S. parasanguinis. | |
Enterococcus species | E. faecium | Maurya et al., 2021 [85] | Sludge samples | 1 isolate | Tube assay method: biofilms were measured based on optical density | ·· | E. faecium biofilm formation was significantly influenced by physiological conditions. |
E. faecalis | Elhadidy and Zahran, 2014 [84] | Bovine mastitis milk samples | 3 strains | Semi-quantitative adherence assay: biofilms were measured based on optical density | ·· | Growth in milk enhanced biofilm formation of E. faecalis. | |
Lactic acid bacteria | Lb. rhamnosus, Lactococcus. lactis subsp. Lactis, Lb. plantarum, Lb. paracasei subsp. Paracasei, Lb. brevis, and Lb. buchneri | Wallis, Krömker and Paduch, 2018 [86] | American Type Culture Collection; bovine milk samples; animal bedding samples | 13 strains | Optical density | ·· | Biofilm formation was observed in all tested strains. |
Lactococcus spp. and Lactobacillus sp. | Zijnge et al., 2010 [87] | Human dental plaque | Not described | Fluorescent in situ hybridization | ·· | Lactobacillus sp. was the main contributor to human oral microbial biofilms. |
4.3. Bacterial Detection in Non-Lactating Mammary Glands and in Pre-Colostrum
5. Evidence for the “Repeated-Cycle Batch Fermentation” Model
6. Knowledge Gaps
7. Weighing the Evidence
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
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Xu, R.; McLoughlin, G.; Nicol, M.; Geddes, D.; Stinson, L. Residents or Tourists: Is the Lactating Mammary Gland Colonized by Residential Microbiota? Microorganisms 2024, 12, 1009. https://doi.org/10.3390/microorganisms12051009
Xu R, McLoughlin G, Nicol M, Geddes D, Stinson L. Residents or Tourists: Is the Lactating Mammary Gland Colonized by Residential Microbiota? Microorganisms. 2024; 12(5):1009. https://doi.org/10.3390/microorganisms12051009
Chicago/Turabian StyleXu, Ruomei, Grace McLoughlin, Mark Nicol, Donna Geddes, and Lisa Stinson. 2024. "Residents or Tourists: Is the Lactating Mammary Gland Colonized by Residential Microbiota?" Microorganisms 12, no. 5: 1009. https://doi.org/10.3390/microorganisms12051009
APA StyleXu, R., McLoughlin, G., Nicol, M., Geddes, D., & Stinson, L. (2024). Residents or Tourists: Is the Lactating Mammary Gland Colonized by Residential Microbiota? Microorganisms, 12(5), 1009. https://doi.org/10.3390/microorganisms12051009