Screening microbiota for effects on host tissues.

cytotoxicity microfluidics skin microbiome

Journal

Biotechnology and bioengineering
ISSN: 1097-0290
Titre abrégé: Biotechnol Bioeng
Pays: United States
ID NLM: 7502021

Informations de publication

Date de publication:
06 2023
Historique:
revised: 20 02 2023
received: 27 09 2022
accepted: 23 02 2023
medline: 15 5 2023
pubmed: 26 2 2023
entrez: 25 2 2023
Statut: ppublish

Résumé

The assembly and function of microbial communities depends on many factors including the local environment and the metabolic properties of the colonizing organisms. Chemical communications or other secreted factors also play a role and are used by different microbial strains both cooperatively and competitively. The spectrum of microbial secretions have various effects on the microbe's respective hosts, both positive and negative. Thus, characterizing the roles of microbial community members and their secretions can yield key mechanistic insights into microbiome function and can lead to new intervention strategies. Focusing on the simple, yet important functional impact of toxicity, we quantify supernatant dosage responses with image data and examine the morphological effects of microbial secretions on skin-associated host cells. Since the diversity of microbial communities, coupled with the multiplicity of host tissues requires scalable methods, we develop and demonstrate a microfluidic device that enables high-content screening of microbial secretion effects on adherent cell types.

Identifiants

pubmed: 36829297
doi: 10.1002/bit.28363
doi:

Types de publication

Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1614-1622

Informations de copyright

© 2023 The Authors. Biotechnology and Bioengineering published by Wiley Periodicals LLC.

Références

Abisado, R. G., Benomar, S., Klaus, J. R., Dandekar, A. A., & Chandler, J. R. (2018). Bacterial quorum sensing and microbial community interactions. mBio, 9(3), e02331-17. https://doi.org/10.1128/MBIO.02331-17/ASSET/D7A06673-524F-46B2-B0E2-DBA0A8744368/ASSETS/GRAPHIC/MBO0031839030001.JPEG
Brown, M. M., & Horswill, A. R. (2020). Staphylococcus epidermidis-Skin friend or foe. PLoS Pathogens, 16(11), e1009026. https://doi.org/10.1371/JOURNAL.PPAT.1009026
Cao, J., Chande, C., & Köhler, J. M. (2022). Microtoxicology by microfluidic instrumentation: A review. Lab on a Chip, 22(14), 2600-2623. https://doi.org/10.1039/D2LC00268J
Cao, X., Hamilton, J. J., & Venturelli, O. S. (2019). Understanding and engineering distributed biochemical pathways in microbial communities. Biochemistry, 58(2), 94-107. https://doi.org/10.1021/acs.biochem.8b01006
Carper, D. L., Weston, D. J., Barde, A., Timm, C. M., Lu, T.-Y., Burdick, L. H., Jawdy, S. S., Klingeman, D. M., Robeson, M. S., Veach, A. M., Cregger, M. A., Kalluri, U. C., Schadt, C. W., Podar, M., Doktycz, M. J., & Pelletier, D. A. (2021). Cultivating the bacterial microbiota of populus roots. mSystems, 6(3), e01306-20. https://doi.org/10.1128/msystems.01306-20
Compant, S., Samad, A., Faist, H., & Sessitsch, A. (2019). A review on the plant microbiome: Ecology, functions, and emerging trends in microbial application. Journal of Advanced Research, 19, 29-37. https://doi.org/10.1016/j.jare.2019.03.004
Davis, C. D. (2016). The gut microbiome and its role in obesity. Nutrition Today, 51(4), 167-174. https://doi.org/10.1097/NT.0000000000000167
Dinges, M. M., Orwin, P. M., & Schlievert, P. M. (2000). Exotoxins of Staphylococcus aureus. Clinical Microbiology Reviews, 13(1), 16-34. https://doi.org/10.1128/CMR.13.1.16-34.2000
Drenkard, E., & Ausubel, F. M. (2002). Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature, 416(6882), 740-743. https://doi.org/10.1038/416740a
Fond, G., Boukouaci, W., Chevalier, G., Regnault, A., Eberl, G., Hamdani, N., Dickerson, F., Macgregor, A., Boyer, L., Dargel, A., Oliveira, J., Tamouza, R., & Leboyer, M. (2015). The “psychomicrobiotic”: Targeting microbiota in major psychiatric disorders: A systematic review. Pathologie Biologie, 63(1), 35-42. https://doi.org/10.1016/J.PATBIO.2014.10.003
Funke, G., Lawson, P. A., Bernard, K. A., & Collins, M. D. (1996). Most Corynebacterium xerosis strains identified in the routine clinical laboratory correspond to Corynebacterium amycolatum. Journal of Clinical Microbiology, 34(5), 1124-1128.
Gage, D. J. (2004). Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiology and Molecular Biology Reviews, 68(2), 280-300. https://doi.org/10.1128/MMBR.68.2.280-300.2004/ASSET/A25A16E1-90DD-4726-8118-EDE3CD3F634E/ASSETS/GRAPHIC/ZMR0020420540007.JPEG
Greenblum, S., Turnbaugh, P. J., & Borenstein, E. (2012). Metagenomic systems biology of the human gut microbiome reveals topological shifts associated with obesity and inflammatory bowel disease. Proceedings of the National Academy of Sciences, 109(2), 594-599. https://doi.org/10.1073/PNAS.1116053109/SUPPL_FILE/SAPP.PDF
Hansen, R. H., Timm, A. C., Timm, C. M., Bible, A. N., Morrell-Falvey, J. L., Pelletier, D. A., Simpson, M. L., Doktycz, M. J., & Retterer, S. T. (2016). Stochastic assembly of bacteria in microwell arrays reveals the importance of confinement in community development. PLoS One, 11(5), e0155080. https://doi.org/10.1371/journal.pone.0155080
Inda, M. E., Broset, E., Lu, T. K., & de la Fuente-Nunez, C. (2019). Emerging frontiers in microbiome engineering. Trends in Immunology, 40(10), 952-973. https://doi.org/10.1016/j.it.2019.08.007
Ishida, T., Shimamoto, T., Ozaki, N., Takaki, S., Kuchimaru, T., Kizaka-Kondoh, S., & Omata, T. (2016). Investigation of the influence of glucose concentration on cancer cells by using a microfluidic gradient generator without the induction of large shear stress. Micromachines, 7(9), 155. https://doi.org/10.3390/mi7090155
Korgaonkar, A., Trivedi, U., Rumbaugh, K. P., & Whiteley, M. (2013). Community surveillance enhances Pseudomonas aeruginosa virulence during polymicrobial infection. Proceedings of the National Academy of Sciences, 110(3), 1059-1064. https://doi.org/10.1073/pnas.1214550110
Lemoine, L., Bayrambey, D., Roloff, A., Hutzler, C., Luch, A., & Tralau, T. (2021). Commensal-related changes in the epidermal barrier function lead to alterations in the benzo[a]pyrene metabolite profile and its distribution in 3D skin. mBio, 12(5), e01223-21. https://doi.org/10.1128/MBIO.01223-21/SUPPL_FILE/MBIO.01223-21-SF003.JPG
Leyden, J. J. (1993). Progression of interdigital infections from simplex to complex. Journal of the American Academy of Dermatology, 28(5), S7-S11. https://doi.org/10.1016/S0190-9622(09)80301-0
Li, B., Selmi, C., Tang, R., Gershwin, M. E., & Ma, X. (2018). The microbiome and autoimmunity: A paradigm from the gut-liver axis. Cellular & Molecular Immunology, 15(6), 595-609. https://doi.org/10.1038/cmi.2018.7
Lim, S. K., Kwon, M. S., Lee, J., Oh, Y. J., Jang, J. Y., Lee, J. H., Park, H. W., Nam, Y. D., Seo, M. J., Roh, S. W., & Choi, H. J. (2017). Weissella cibaria WIKIM28 ameliorates atopic dermatitis-like skin lesions by inducing tolerogenic dendritic cells and regulatory T cells in BALB/c mice. Scientific Reports, 7(July 2016), 40040. https://doi.org/10.1038/srep40040
Loomis, K. H., Wu, S. K., Ernlund, A., Zudock, K., Reno, A., Blount, K., & Karig, D. K. (2021). A mixed community of skin microbiome representatives influences cutaneous processes more than individual members. Microbiome, 9(1), 22. https://doi.org/10.1186/s40168-020-00963-1
Lu, X., Ye, Y., Zhang, Y., & Sun, X. (2021). Current research progress of mammalian cell-based biosensors on the detection of foodborne pathogens and toxins. Critical Reviews in Food Science and Nutrition, 61(22), 3819-3835. https://doi.org/10.1080/10408398.2020.1809341
Luna, R. A., & Foster, J. A. (2015). Gut brain axis: Diet microbiota interactions and implications for modulation of anxiety and depression. Current Opinion in Biotechnology, 32, 35-41. https://doi.org/10.1016/J.COPBIO.2014.10.007
Mann, E. E., & Wozniak, D. J. (2012). Pseudomonas biofilm matrix composition and niche biology. FEMS Microbiology Reviews, 36(4), 893-916. https://doi.org/10.1111/J.1574-6976.2011.00322.X
Marietta, E., Horwath, I., Balakrishnan, B., & Taneja, V. (2019). Role of the intestinal microbiome in autoimmune diseases and its use in treatments. Cellular Immunology, 339(September 2018), 50-58. https://doi.org/10.1016/j.cellimm.2018.10.005
McLean, M. H., Dieguez, D., Miller, L. M., & Young, H. A. (2015). Does the microbiota play a role in the pathogenesis of autoimmune diseases. Gut, 64(2), 332-341. https://doi.org/10.1136/gutjnl-2014-308514
McNally, L., Viana, M., & Brown, S. P. (2014). Cooperative secretions facilitate host range expansion in bacteria. Nature Communications, 5, 4594. https://doi.org/10.1038/ncomms5594
Moran, C. P., & Shanahan, F. (2014). Gut microbiota and obesity: Role in aetiology and potential therapeutic target. Best Practice & Research Clinical Gastroenterology, 28(4), 585-597. https://doi.org/10.1016/J.BPG.2014.07.005
Nogueira, T., Rankin, D. J., Touchon, M., Taddei, F., Brown, S. P., & Rocha, E. P. C. (2009). Horizontal gene transfer of the secretome drives the evolution of bacterial cooperation and virulence. Current Biology, 19(20), 1683-1691. https://doi.org/10.1016/j.cub.2009.08.056
O'Neill, A. M., & Gallo, R. L. (2018). Host-microbiome interactions and recent progress into understanding the biology of acne vulgaris. Microbiome, 6(1), 177. https://doi.org/10.1186/s40168-018-0558-5
Otto, M. (2009). Staphylococcus epidermidis-The “accidental” pathogen. Nature Reviews Microbiology, 7(8), 555-567. https://doi.org/10.1038/nrmicro2182
Pistone, D., Meroni, G., Panelli, S., D'auria, E., Acunzo, M., Pasala, A. R., Zuccotti, G. V., Bandi, C., & Drago, L. (2021). A journey on the skin microbiome: Pitfalls and opportunities. International Journal of Molecular Sciences, 22(18), 9846. https://doi.org/10.3390/IJMS22189846
den Reijer, P. M., Haisma, E. M., Lemmens-Den Toom, N. A., Willemse, J., Koning, R. A., Demmers, J. A. A., Dekkers, D. H. W., Rijkers, E., El Ghalbzouri, A., Nibbering, P. H., & Van Wamel, W. (2016). Detection of alpha-toxin and other virulence factors in biofilms of Staphylococcus aureus on polystyrene and a human epidermal model. PLoS One, 11(1), e0145722. https://doi.org/10.1371/journal.pone.0145722
Reverté, L., Soliño, L., Carnicer, O., Diogène, J., & Campàs, M. (2014). Alternative methods for the detection of emerging marine toxins: Biosensors, biochemical assays and cell-based assays. Marine Drugs, 12(12), 5719-5763. https://doi.org/10.3390/md12125719
Tan, H. Y., & Toh, Y. C. (2020). What can microfluidics do for human microbiome research. Biomicrofluidics, 14(4), 51303. https://doi.org/10.1063/5.0012185
Tham, E. H., Koh, E., Common, J. E. A., & Hwang, I. Y. (2020). Biotherapeutic approaches in atopic dermatitis. Biotechnology Journal, 15(10), 1900322. https://doi.org/10.1002/biot.201900322
Tian, P., Xu, B., Sun, H., Li, X., Li, Z., & Wei, P. (2014). Isolation and gut microbiota modulation of antibiotic-resistant probiotics from human feces. Diagnostic Microbiology and Infectious Disease, 79(4), 405-412. https://doi.org/10.1016/J.DIAGMICROBIO.2014.04.002
Timm, A. C., Halsted, M. C., Wilmoth, J. L., & Retterer, S. T. (2017). Assembly and tracking of microbial community development within a microwell array platform. Journal of visualized experiments: JoVE, 2017(124), e55701. https://doi.org/10.3791/55701
Timm, A. C., Warrick, J. W., & Yin, J. (2017). Quantitative profiling of innate immune activation by viral infection in single cells. Integrative Biology, 9(9), 782-791. https://doi.org/10.1039/c7ib00082k
Timm, C. M., Carter, K. R., Carrell, A. A., Jun, S.-R., Jawdy, S. S., Vélez, J. M., Gunter, L. E., Yang, Z., Nookaew, I., Engle, N. L., Lu, T.-Y. S., Schadt, C. W., Tschaplinski, T. J., Doktycz, M. J., Tuskan, G. A., Pelletier, D. A., & Weston, D. J. (2018). Abiotic stresses shift belowground populus-associated bacteria toward a core stress microbiome. mSystems, 3(1), e00070-17.
Timm, C. M., Loomis, K., Stone, W., Mehoke, T., Brensinger, B., Pellicore, M., Staniczenko, P. P. A., Charles, C., Nayak, S., & Karig, D. K. (2020). Isolation and characterization of diverse microbial representatives from the human skin microbiome. Microbiome, 8(1), 58. https://doi.org/10.1186/s40168-020-00831-y
Turnbaugh, P. J., Hamady, M., Yatsunenko, T., Cantarel, B. L., Duncan, A., Ley, R. E., Sogin, M. L., Jones, W. J., Roe, B. A., Affourtit, J. P., Egholm, M., Henrissat, B., Heath, A. C., Knight, R., & Gordon, J. I. (2009). A core gut microbiome in obese and lean twins. Nature, 457(7228), 480-484. https://doi.org/10.1038/nature07540
Valle, N. M. E., Nucci, M. P., Alves, A. H., Rodrigues, L. D., Mamani, J. B., Oliveira, F. A., Lopes, C. S., Lopes, A. T., Carreño, M. N. P., & Gamarra, L. F. (2022). Advances in concentration gradient generation approaches in a microfluidic device for toxicity analysis. Cells, 11(19), 3101. https://doi.org/10.3390/cells11193101
Xu, L., Huang, H., Wei, W., Zhong, Y., Tang, B., Yuan, H., Zhu, L., Huang, W., Ge, M., Yang, S., Zheng, H., Jiang, W., Chen, D., Zhao, G. P., & Zhao, W. (2014). Complete genome sequence and comparative genomic analyses of the vancomycin-producing Amycolatopsis orientalis. BMC Genomics, 15(1), 363. https://doi.org/10.1186/1471-2164-15-363/FIGURES/6
Ye, Y., Guo, H., & Sun, X. (2019). Recent progress on cell-based biosensors for analysis of food safety and quality control. Biosensors and Bioelectronics, 126(October 2018), 389-404. https://doi.org/10.1016/j.bios.2018.10.039
Zitvogel, L., Galluzzi, L., Viaud, S., Vétizou, M., Daillère, R., Merad, M., & Kroemer, G. (2015). Cancer and the gut microbiota: An unexpected link. Science Translational Medicine, 7(271), 271-272. https://doi.org/10.1126/scitranslmed.3010473

Auteurs

Andrea C Timm (AC)

Research and Exploratory Development Department, Johns Hopkins University Applied Physics Laboratory, Laurel, Maryland, USA.

Bryan Brensinger (B)

Research and Exploratory Development Department, Johns Hopkins University Applied Physics Laboratory, Laurel, Maryland, USA.

Meaghan Hart (M)

Research and Exploratory Development Department, Johns Hopkins University Applied Physics Laboratory, Laurel, Maryland, USA.

Collin Timm (C)

Research and Exploratory Development Department, Johns Hopkins University Applied Physics Laboratory, Laurel, Maryland, USA.

David Karig (D)

Bioengineering Department, Clemson University, Clemson, South Carolina, USA.

Articles similaires

Populus Soil Microbiology Soil Microbiota Fungi
Aerosols Humans Decontamination Air Microbiology Masks
Coal Metagenome Phylogeny Bacteria Genome, Bacterial
Semiconductors Photosynthesis Polymers Carbon Dioxide Bacteria

Classifications MeSH