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Center for Biofilm Engineering

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Coordinates: 45°39′57″N 111°02′47″W / 45.66583°N 111.04639°W / 45.66583; -111.04639 (Engineering and Physical Sciences Bldg, Montana State University)
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Center for Biofilm Engineering
Montana State University’s Engineering and Physical Science Building, home of Center for Biofilm Engineering
Parent institutionMontana State University
Established15 April 1990 (1990-04-15)[1]
MissionAdvance the basic knowledge, technology and education required to understand, control and exploit biofilm processes
DirectorMatthew W. Fields (2015–current)
Philip S. Stewart (2005–2015)
John W. Costerton (1993–2004)
William G. Characklis (1990–92)
Formerly calledCenter for Interfacial Microbial Process Engineering[2]
Location
Bozeman
,
Montana
,
United States
Coordinates45°39′57″N 111°02′47″W / 45.66583°N 111.04639°W / 45.66583; -111.04639 (Engineering and Physical Sciences Bldg, Montana State University)
Websitewww.biofilm.montana.edu

The Center for Biofilm Engineering (CBE) is an interdisciplinary research, education, and technology transfer institution located on the central campus of Montana State University in Bozeman, Montana. The center was founded in April 1990 as the Center for Interfacial Microbial Process Engineering with a grant from the Engineering Research Centers (ERC) program of the National Science Foundation (NSF).[3] The CBE integrates faculty from multiple university departments to lead multidisciplinary research teams—including graduate and undergraduate students—to advance fundamental biofilm knowledge, develop beneficial uses for microbial biofilms, and find solutions to industrially relevant biofilm problems. The center tackles biofilm issues including chronic wounds, bioremediation, and microbial corrosion through cross-disciplinary research and education among engineers, microbiologists and industry.[4][5]

History

The center originated as the Institute for Chemical and Biological Process Analysis (IPA) in 1983.[1] In 1990, the center became a national ERC as the Center for Interfacial Microbial Process Engineering based on a $7.2 million grant from the NSF.[2] In 1993 the center assumed its current name-Center for Biofilm Engineering. The original grants expired in 2001 and the center became self-sufficient. The center celebrated its 25th anniversary as an NSF ERC in 2015.

Institute for Chemical and Biological Process Analysis (1979–1990)

In 1979 W.G. (Bill) Characklis came to Montana State University from Rice University as a professor in civil (environmental) and chemical engineering. He assembled a multidisciplinary team of engineers, microbiologists and chemists to study the processes and effects of microbial growth at interfaces[6] He established a cross-disciplinary environmental biotechnology institute to address the needs of industry in the areas of biofouling, microbial corrosion and biofilm technology.[1] The Institute for Chemical and Biological Process Analysis (IPA) was chartered by the Montana Board of Regents in 1983 within the Montana State University College of Engineering. Bill Characklis was its first director. The IPA provided the foundation for eventual Engineering Research Center status in several ways. The IPA conducted fundamental research, development, and testing for industry and government agencies and it pursued biofilm projects that crossed traditional scientific discipline boundaries.[7] The IPA established an Industrial Associates membership program and by 1989 the program had 12 participating members, each contributing $10,000 annually to the center. Membership benefits provided them the opportunity to assist in critiquing and defining the IPA research programs. Members included oil/gas/power companies, a chemical manufacturer, a pulp and paper company and partnership with the Idaho National Engineering Laboratory.[8]

Center for Interfacial Microbial Process Engineering (1990–1993)

photograph of microscope
Leica confocal microscope systems

In 1989, the IPA applied to the NSF for Engineering Research Center status, which was granted in April 1990.[3] The Center for Interfacial Microbial Process Engineering was established as one of three national Engineering Research Centers out of 48 applicants.[9] As an ERC, the new organization was charged with building a cross-disciplinary research and education program at Montana State University, as well as increasing U.S. industrial competitiveness in biofilm related technologies. The center's charter mandated that research, education, and technology transfer programs would be fully integrated within the center's program planning. The Industrial Associates program continued to be used as a mechanism for the center to get information from industry about significant biofilm-related problems and collaborate on center research initiatives designed to address biofilm issues. The center’s education program recruited students to participate on interdisciplinary research teams and to interact with industry representatives.[1]

The provision of $7.2 million in grants from the NSF during the first five years enabled the expansion of center research into new areas, notably bioremediation and biohydrometallurgy. The center's industrial focus expanded from biofilm control and mitigation to include positive use of biofilm processes to break up soil and water contaminants as well as extracting minerals from low-grade ores.[1] Center projects were designed to span scales of inquiry from fundamental bench-scale to applied field-scale experiments. These projects enabled the continued development of microsensors to measure gradients of gases and pH within biofilm communities,[10] microscopy to elucidate physiological activity of community organisms[11] and modeling to predict biofilm behavior.[12]

Center for Biofilm Engineering (1993–present)

In 1992, two years after its establishment, the center's first director, Bill Characklis, died. Montana State University signaled its commitment to the center by hiring J.W. (Bill) Costerton, a professor of microbiology from the University of Calgary, as Executive Director and James Bryers, a professor of biochemical engineering from Duke University, as Director of Research for the center. In 1993 the center’s name was changed to Center for Biofilm Engineering (CBE).[13]

Under Costerton's direction the center continued to fulfil its charter and began expanding its scope of inquiry. Costerton encouraged exploration of the bioelectric effect,[14] the phenomenon of cell-cell signaling and its relation to biofilm structure[15] and subsurface biobarrier technologies to protect water and soils from mining contamination.[16] Industrial interest and membership grew in response to more diversified research topics. By 1996 Industrial Associate membership had grown to 19 diversified members including members representing water treatment, mining, government labs, specialty chemicals, consumer products, and oil/energy companies.[17] In June 1996 the National Science Foundation renewed its commitment to the Center for Biofilm Engineering with a new five year grant of $7.6 million.[4]

In 1996 the national profile of the CBE and biofilm research was on the rise. Numerous scientific and mass media publications began to address biofilm technology in ernest. An article in the September 1996 issue of Science, entitled "Biofilms Invade Microbiology" featured the work and history of the Center for Biofilm Engineering.[4] Other magazines and newspapers featuring biofilms and CBE research included New Scientist (cover article, August 31, 1996),[18] Science News (April 26, 1997),[19] the Chicago Sun-Times (May 17, 1998),[20] Science (March 19, 1999),[21] Businessweek (September 12, 1999),[22] Knight Ridder/Tribune News Service (January 7, 2000),[23] Nature (November 16, 2000)[24] and The Boston Globe (May 28, 2002).[25] In 2001 Costerton and CBE Deputy Director Philip S. Stewart authored a biofilm article "Battling Biofilms" published in Scientific American (July 1, 2001)[26]

Self-sufficiency (2001–)

The NSF ERC program was designed to create institutional centers that would be self-sufficient within ten years. The Center for Biofilm Engineering at Montana State University started planning for self-sufficiency in 1998 through the establishment of a Self-sufficiency Task Force at the university. The center achieved self-sufficiency in 2001 and continues to be funded in part through federal and private grants with continued emphasis on providing value to the Industrial Associates, and support from Montana State University and the State of Montana.[27] In 2005 Philip S. Stewart, a professor of chemical and biological engineering, was selected to be the third CBE Director. Stewart, who had participated as a CBE faculty member since 1991, was a leading expert on antimicrobials and biofilm control.[28][29][30] Under Stewart’s tenure, CBE has grown in affiliated faculty numbers, industrial membership, the number of testing and industry-sponsored projects, and the participation of undergraduate and graduate students. The center is one of 24 self-sustaining Engineering Research Centers in the National Science Foundation program.[31]

Programs

Research program

Image of researcher with chemistry equipment in laboratory
Anaerobic experiment station

The center's biofilm research program was established in the 1980s with a focus on environmental bioengineering, interdisciplinary investigation, and industrial participation. Faculty expertise from civil/environmental engineering, mathematics, microbiology, chemical and biological engineering, chemistry and biochemistry, mechanical and industrial engineering, computer science, electrical engineering, and statistics contributes to hypothesis development and experimental design. The center conducts research that includes multiple scales of observation, from molecular to industrial field-scale, with projects that cover both fundamental and applied topics. CBE research teams have been part of numerous groundbreaking advances in biofilm science and technology including: quorum sensing,[32] permeability (earth sciences),[33] biomineralization,[34] antimicrobial tolerance,[28] viscoelasticity,[35] detachment,[36] standardized biofilm methods,[37] chronic wounds,[38] algae fuel,[39] microbial corrosion,[40] sulfate-reducing bacteria,[41] and biofilm structure and function.[42] CBE research has been published in high-profile peer-reviewed journals including: Nature,[43] The Lancet,[44] Science,[45][46] JAMA,[47] PNAS,[48][49] EMBO Journal,[50] ISME Journal,[51][52] Nature Reviews Microbiology[53][54] and Physical Review Letters.[55] By 2014, CBE authors had published 1,024 peer-reviewed papers.[56] The center has provided over 17 cover images related to biofilms for peer-reviewed journals.[57]

Applied research topics addressed by the center in 2014 included:[5]

  • Biofilm control strategies (antimicrobial efficacy, biocides, bioactive compounds, disinfectant efficacy)
  • Energy solutions (biofuels, coalbed methane production, microbial fuel cells)
  • Environmental technologies (bioremediation, wetlands, biomineralization, mining, carbon sequestration)
  • Health/medical biofilms (chronic wounds, catheter infections, oral health)
  • Industrial systems and processes (biofouling, microbial corrosion, product contamination)
  • Standardized methods (product claims, regulatory issues, ASTM methods development)
  • Water systems (drinking water quality, premise plumbing, water treatment, distribution systems)

Other research topics in 2014 included:

The center's standing in the international research community and its encouragement of collaboration regularly attracts visiting students and faculty from numerous institutions in the U.S. and foreign countries. From 1990 to 2014, over 265 visiting researchers from more than 30 countries and 38 U.S. states spent from several weeks to a year or more studying biofilms in CBE laboratories. In 2014, 18 visiting scientists and engineers conducted research at CBE.[58]

Industry programs

The center's Industrial Associates program provides access to center information, expertise, training and other benefits for a yearly subscription fee. The program was started in 1983 with the creation of the Institute for Chemical and Biological Process Analysis.[7] CBE’s Standardized Biofilm Methods research group (SBM) focuses on issues of interest to companies developing new products addressing biofilm formation. Researchers develop, refine, and publish quantitative methods for growing, treating, sampling, and analyzing biofilm bacteria. SBM laboratory members work with international standard setting organizations to secure approval of biofilm methods by the standard setting community.[59] Under a contract with the U.S. Environmental Protection Agency, the SBM conducts laboratory research to support the development and standardization of test methods for measuring the performance of antimicrobial products—including those for biofilm bacteria—and provide statistical services related to EPA's Office of Pesticide Programs Antimicrobial Testing Program.[60]

In 2013 CBE Director Phil Stewart and CBE Industrial Coordinator Paul Sturman worked to partner with the U.S. Food and Drug Administration (FDA) to co-sponsor a one-day workshop on biofilms. The resulting workshop, "Biofilms, Medical Devices and Anti-Biofilm Technology: Challenges and Opportunities," was held on the FDA White Oak campus on February 20, 2014.[61][62] A follow-up CBE-hosted meeting on February 11, 2015 in College Park, Maryland, titled "Anti-Biofilm Technologies: Pathways to Productivity" was held to continue fostering scientific dialog between U.S. government agencies, industry and academia.[63]

Member companies have represented several industrial categories including energy/petroleum, chemicals/specialty chemicals, household/consumer products, medical/healthcare, testing laboratories, government laboratories, water, pulp and paper, and mining. Members range from large Fortune 500 international corporations to small start-up companies.

2016 CBE Industrial Associates[58]
3M Ecolab Procter & Gamble
Accuratus Lab Services ICU Medical SANUWAVE Health
Acelity Lonza Sealed Air
American Chemet Masco Sterilex
BASF NASA STERIS
Baxter Healthcare NCH The Sherwin-Williams Company
Church & Dwight Next Science W.L. Gore & Associates
Dow Corning Novozymes Zimmer Biomet
Dow Microbial Control PPG

Education program

photo of microscopes in laboratory
Optical microscopy laboratory

Graduate and undergraduate students participate in collaborative, interdisciplinary research at the center. Students work under the guidance of multidisciplinary faculty to solve problems associated with biofilms in medical, industrial, and environmental contexts. Faculty and students from the following MSU departments and programs participated in the center's research from 2011 to 2014.[64]

Undergraduate studies

Undergraduate students are hired as undergraduate research assistants and work in CBE laboratories as members of research teams on interdisciplinary biofilm projects. CBE undergraduates are encouraged to acquire competence in laboratory skills, experimental design and group communication. By 2014, over 730 undergraduates from 11 disciplines had worked on laboratory biofilm projects under the direction of CBE-affiliated faculty members. Thirty-four of 55 undergraduates (62%) in the 2013-14 academic year were female.[58][64]

Graduate studies

Graduate students pursue their degree in a discipline offered through one of the science, agriculture, or engineering departments at Montana State University while they conduct their research in CBE laboratories. Student graduate committees are typically interdisciplinary. The student and graduate committee members select coursework appropriate for the student’s interests and degree program. Engineering students are encouraged to take microbiology courses; science students are encouraged to take relevant engineering coursework. Graduate students acquire experience by designing and performing research that crosses traditional academic discipline boundaries and has direct impact on current environmental, industrial, and medical issues. Students work on projects that range from fundamental to applied topics. In addition, the CBE’s Industrial Associates program brings students into working relationships with potential employers. Graduate students are encouraged to develop their communication and leadership skills by presenting at research conferences, mentoring undergraduate students, organizing the CBE’s seminar series, and assisting with outreach efforts.[65] By the end of 2014, over 230 graduate students had received advanced degrees (143 master’s and 89 doctorate degrees) based on their work at the center. During the 2013-2014 academic year 29 of the 55 active graduate student researchers (53%) were female.[58][64]

See also

Notes

  1. ^ a b c d e Report on Research 1990, Montana State University (Report). pp. 10–11.
  2. ^ a b "Environment/Ecology Grants". The Scientist. 4 (24). Midland, Ontario, Canada: LabX Media Group: 25. December 10, 1990. Retrieved 2015-02-27. To establish new Center for Interfacial Microbial Process Engineering; work will focus on biofouling and biocorrosion, bioremediation, and biohydrometallurgy. $7.2 million from NSF to Montana State University, Bozeman.
  3. ^ a b "Original Charter" (pdf). National Science Foundation. April 15, 1990. Retrieved 2015-02-27.
  4. ^ a b c Potera, Carol (September 27, 1996). "Biofilms Invade Microbiology-Linking Microbiology and Engineering". Science. 273 (5283). American Association for the Advancement of Science: 1795–1796. doi:10.1126/science.273.5283.1795. JSTOR 2891076.
  5. ^ a b "CBE Research Program". Montana State University. Retrieved 2015-02-27.
  6. ^ "Center for Interfacial Microbial Process Engineering Newsletter". InProcess. Fall 1992.
  7. ^ a b Brochure: "Montana State University introduces The Institute for Biological and Chemical Process Analysis." 1983
  8. ^ Report: "Strategic Plan of the Institute for Biological and Chemical Process Analysis." February 1989, p 50.
  9. ^ Strategic Plan of the Institute for Biological and Chemical Process Analysis (Report). February 1989. p. 50.
  10. ^ Lewandowski Z, Lee W, Characklis WG, Little BJ, "Dissolved oxygen and pH microelectrode measurements at water-immersed metal surfaces," Corrosion Science, 1989;45(2):92-98.
  11. ^ "Spatial variations in growth rate within Klebsiella pneumoniae colonies and biofilm". Biotechnology Progress. 12 (3). American Institute of Chemical Engineers: 316–321. 1996. doi:10.1021/bp9600243. Retrieved 2015-03-06. {{cite journal}}: Unknown parameter |authors= ignored (help)
  12. ^ "Diffusion and reaction within porous packing media: A phenomenological model". Biotechnology and Bioengineering. 41 (10). Wiley Periodicals, Inc.: 947–956 April 25, 1993. doi:10.1002/bit.260411005. Retrieved 2015-03-06. {{cite journal}}: Unknown parameter |authors= ignored (help)
  13. ^ Center for Biofilm Engineering News, 1993 April;1(1):1-3.
  14. ^ "Mechanism of the electrical enhancement of the efficacy of antibiotics in killing biofilm bacteria". Antimicrobial Agents and Chemotherapy. 38 (12). American Society for Microbiology: 2803–2809. December 1994. doi:10.1128/aac.38.12.2803. Retrieved 2015-02-28. {{cite journal}}: Unknown parameter |authors= ignored (help)
  15. ^ "Regulation of the alginate biosynthesis gene algC in Pseudomonas aeruginosa during biofilm development in continuous culture" (pdf). Applied and Environmental Microbiology. 61 (3). American Society for Microbiology: 860–7. March 1995. PMC 167351. PMID 7793920. Retrieved 2015-03-02. {{cite journal}}: Unknown parameter |authors= ignored (help)
  16. ^ "Evaluation of subsurface biobarrier formation and persistence" (pdf). Proceedings of the 10th Annual Conference on Hazardous Waste Research, Manhattan, KS.: 82–91. May 24, 1995. Retrieved 2015-03-06. {{cite journal}}: Unknown parameter |authors= ignored (help)
  17. ^ Center for Biofilm Engineering Year Seven Report and Renewal Proposal, February 1997; Table 9.3.
  18. ^ Coghlan, Andy (August 31, 1996). "Slime City". New Scientist (2045): 32–36. ISSN 0262-4079. Retrieved 2015-03-01.
  19. ^ Wu, Corinna (April 26, 1997). "Material Gives Bacterial Films the Heave-Ho". Science News. Retrieved 2015-03-01.
  20. ^ Sternberg, Steve (May 17, 1998). "The tooth of the matter: Dental infections implicated in other illnesses". Chicago Sun-Times.
  21. ^ Potera, Carol (March 19, 1999). "Forging a link between biofilms and disease". Science. 283 (5409). American Association for the Advancement of Science: 1837–1839. doi:10.1126/science.283.5409.1837. JSTOR 2896613.
  22. ^ Licking, Ellen (September 12, 1999). "Getting a grip on bacterial slime". Businessweek. Retrieved 2015-03-01.
  23. ^ Boyd,Robert S. (January 7, 2000). "'Slimy, horrible biofilms' pervade everyday life". Knight Ridder/Tribune News Service. Retrieved 2015-03-01.
  24. ^ Chicurel, Marina (November 16, 2000). "Slime Busters". Nature. 408 (408): 284–286. doi:10.1038/35042737. Retrieved 2015-03-01.
  25. ^ Delude, Cathryn Delude (May 28, 2002). "Culprit in ear infections is a 'biofilm' that protects bacteria". The Boston Globe. Retrieved 2015-03-01.
  26. ^ "Battling Biofilms" (pdf). Scientific American. 285: 75–81. July 1, 2001. doi:10.1038/scientificamerican0701-74. {{cite journal}}: Unknown parameter |authors= ignored (help)
  27. ^ Center for Biofilm Engineering Final Report. February 2001. p15.
  28. ^ a b "Direct measurement of chlorine penetration into biofilms during disinfection". Applied and Environmental Microbiology. 60 (12): 4339–4344. December 1994. Retrieved 2015-02-27. {{cite journal}}: Unknown parameter |authors= ignored (help)
  29. ^ "A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance". Nature. 426 (6964): 306–310. November 20, 2003. doi:10.1038/nature02122. Retrieved 2015-02-27. {{cite journal}}: Unknown parameter |authors= ignored (help)
  30. ^ "Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin" (pdf). Antimicrobial Agents and Chemotherapy. 47 (1): 317–323. January 2003. doi:10.1128/aac.47.1.317-323.2003. Retrieved 2015-02-27. {{cite journal}}: Unknown parameter |authors= ignored (help)
  31. ^ "ERC Graduated Centers (self-sustaining)". Engineering Research Center Association. Retrieved 2015-02-28.
  32. ^ "The involvement of cell-to-cell signals in the development of a bacterial biofilm". Science. 280 (5361). American Association for the Advancement of Science: 295–298. April 10, 1998. doi:10.1126/science.280.5361.295. JSTOR 2895685. {{cite journal}}: Unknown parameter |authors= ignored (help)
  33. ^ "Influence of biofilm accumulation on porous media hydrodynamics". Environmental Science and Technology. 25 (7). American Chemical Society: 1305–1311. July 1991. doi:10.1021/es00019a013. Retrieved 2015-02-27. {{cite journal}}: Unknown parameter |authors= ignored (help)
  34. ^ "Microbially enhanced carbonate mineralization and the geologic containment of CO2" (PDF). Energy Procedia. 1 (1): 3245–3252. February 2009. doi:10.1016/j.egypro.2009.02.109. Retrieved 2015-02-27. {{cite journal}}: Unknown parameter |authors= ignored (help)
  35. ^ "A viscoelastic fluid description of bacterial biofilm material properties". Biotechnology and Bioengineering. 80 (3). John Wiley & Sons: 289–296. November 5, 2002. doi:10.1002/bit.10376. Retrieved 2015-02-27. {{cite journal}}: Unknown parameter |authors= ignored (help)
  36. ^ Peyton BM, Characklis WG (1993). "A statistical analysis of the effect of substrate utilization and shear stress on the kinetics of biofilm detachment". Biotechnol Bioeng. 41 (7): 728–735. doi:10.1002/bit.260410707.
  37. ^ "Comparative evaluation of biofilm disinfectant efficacy tests". Journal of Microbiolic Methods. 70 (2). Elsevier B.V.: 236–244 August 2007. doi:10.1016/j.mimet.2007.04.010. Retrieved 2015-03-02. {{cite journal}}: Unknown parameter |authors= ignored (help)
  38. ^ "Biofilms in chronic wounds" (pdf). Wound Repair and Regeneration. 16 (1). Wound Healing Society: 37–44. February 2008. doi:10.1111/j.1524-475x.2007.00321.x. Retrieved 2015-03-02. {{cite journal}}: Unknown parameter |authors= ignored (help)
  39. ^ "Sources and resources: Importance of nutrients, resource allocation, and ecology in microalgal cultivation for lipid accumulation" (pdf). Applied Microbiology and Biotechnology. 98 (11). Springer Berlin Heidelberg: 4805–4816. June 2014. doi:10.1007/s00253-014-5694-7. Retrieved 2015-03-03. {{cite journal}}: Unknown parameter |authors= ignored (help)
  40. ^ "Ennoblement of stainless steel by the manganese-depositing bacterium Leptothrix discophora" (pdf). Applied and Environmental Microbiology. 63 (7). American Society for Microbiology: 2502–2506. July 1997. PMC 1389190. PMID 16535635. Retrieved 2015-03-04. {{cite journal}}: Unknown parameter |authors= ignored (help)
  41. ^ Chen CI, Reinsel MA, Mueller RF (1994). "Kinetic investigation of microbial souring in porous media using microbial consortia from oil reservoirs". Biotechnol Bioeng. 44 (3): 263–269. doi:10.1002/bit.260440302.
  42. ^ De Beer D, Stoodley P, Roe F, Lewandowski Z (1994). "Effects of biofilm structures on oxygen distribution and mass transport". Biotechnol Bioeng. 43 (11): 1131–1138. doi:10.1002/bit.260431118.
  43. ^ "A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance". Nature. 426 (6964). Nature Publishing Group: 306–310. November 20, 2003. doi:10.1038/nature02122. Retrieved 2015-03-04. {{cite journal}}: Unknown parameter |authors= ignored (help)
  44. ^ "Antibiotic resistance of bacteria in biofilms" (pdf). Lancet. 358 (9276). Elsevier B.V.: 135–138 July 14, 2001. doi:10.1016/s0140-6736(01)05321-1. Retrieved 2015-03-04. {{cite journal}}: Unknown parameter |authors= ignored (help)
  45. ^ "The involvement of cell-to-cell signals in the development of a bacterial biofilm" (pdf). Science. 280 (5361). American Association for the Advancement of Science: 295–298. April 10, 1998. doi:10.1126/science.280.5361.295. Retrieved 2015-03-04. {{cite journal}}: Unknown parameter |authors= ignored (help)
  46. ^ "Bacterial biofilms: A common cause of persistent infections" (pdf). Science. 284 (5418). American Association for the Advancement of Science: 1318–1322. May 21, 1999. doi:10.1126/science.284.5418.1318. PMID 10334980. Retrieved 2015-03-03. {{cite journal}}: Unknown parameter |authors= ignored (help)
  47. ^ "Mucosal biofilm formation on middle-ear mucosa in the chinchilla model of otitis media". JAMA. 287 (13). American Medical Association: 1710–1715. April 3, 2002. doi:10.1001/jama.287.13.1710. Retrieved 2015-03-03. {{cite journal}}: Unknown parameter |authors= ignored (help)
  48. ^ "Iron induces bimodal population development by Escherichia coli" (pdf). PNAS. 110 (7). National Academy of Sciences: 2629–2634. February 12, 2003. doi:10.1073/pnas.1218703110. PMC 3574911. PMID 23359678. Retrieved 2015-03-03. {{cite journal}}: Unknown parameter |authors= ignored (help)
  49. ^ "Geographic, seasonal, and precipitation chemistry influence on the abundance and activity of biological ice nucleators in rain and snow" (pdf). PNAS. 105 (48). National Academy of Sciences: 18854–18859. December 2, 2008. doi:10.1073/pnas.0809816105. Retrieved 2015-03-03. {{cite journal}}: Unknown parameter |authors= ignored (help)
  50. ^ "Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors" (pdf). The EMBO Journal. 22 (15). The European Molecular Biology Organization: 3803–3815. August 1, 2003. doi:10.1093/emboj/cdg366. PMC 169039. PMID 12881415. Retrieved 2015-03-03. {{cite journal}}: Unknown parameter |authors= ignored (help)
  51. ^ "Impact of elevated nitrate on sulfate-reducing bacteria: A comparative study of Desulfovibrio vulgaris" (pdf). The ISME Journal. 4 (11). International Society for Microbial Ecology: 1386–97. November 2010. doi:10.1038/ismej.2010.59. Retrieved 2015-03-03. {{cite journal}}: Unknown parameter |authors= ignored (help)
  52. ^ "Bacterial community succession during in situ uranium bioremediation: Spatial similarities along controlled flow paths" (pdf). The ISME Journal. 3. International Society for Microbial Ecology: 47–64. 2009. doi:10.1038/ismej.2008.77. Retrieved 2015-03-02. {{cite journal}}: Unknown parameter |authors= ignored (help)
  53. ^ "Physiological heterogeneity in biofilms". Nature Reviews Microbiology. 6 (3). Nature Publishing Group: 199–210. March 2008. doi:10.1038/nrmicro1838. Retrieved 2015-03-03. {{cite journal}}: Unknown parameter |authors= ignored (help)
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  55. ^ "Anomalous fluid transport in porous media induced by biofilm growth" (pdf). Physical Review Letters. 93 (19): 198103. November 5, 2004. doi:10.1103/physrevlett.93.198103. {{cite journal}}: Unknown parameter |authors= ignored (help)
  56. ^ "CBE Publications Database". Montana State University. Retrieved 2015-02-27.
  57. ^ "Research Cover Images". Montana State University. Retrieved 2015-03-05.
  58. ^ a b c d MSU Center for Biofilm Engineering 25 years and growing (pdf) (Report). 2014. pp. 1–24. Retrieved 2015-02-27.
  59. ^ Griffin K (Nov 22, 2013). "CBE faculty member honored by ASTM International". Montana State University. Retrieved 2015-02-27.
  60. ^ Becker, Michael (August 22, 2008). "MSU biofilms research helps set standards for everyday products". MSU News Service. Retrieved 2015-02-27.
  61. ^ "FDA to hold forum on anti-biofilm technology". States News Service. January 24, 2014. Retrieved 20 January 2016.
  62. ^ "Public Workshop – Biofilms, Medical Devices and Anti-Biofilm Technology – Challenges and Opportunities, February 20, 2014". Federal Register Web. Retrieved 2015-02-27.
  63. ^ "Agenda: Anti-Biofilm Technologies: Pathways to Product Development" (pdf). Montana State University. February 20, 2014. Retrieved 2015-02-27.
  64. ^ a b c 2014 CBE APPENDIX, CBE Annual Report (pdf) (Report). MSU Center for Biofilm Engineering. 2014. pp. 16, 19–23. Retrieved 2015-02-27.
  65. ^ "CBE Graduate Education". Montana State University. Retrieved 2015-02-27.
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