Roberto Kolter

Last updated
Roberto Kolter
Born1953
Guatemala
Known for Biofilms, stationary phase, antibiotic biosynthesis
Scientific career
Fields Microbiology, molecular genetics, chemical ecology, molecular microbiology, microbial ecology
Institutions Harvard Medical School
Doctoral advisor Donald Helinski
Other academic advisors Charles Yanofsky
Website http://gasp.med.harvard.edu/

Roberto Kolter is Professor of Microbiology, Emeritus at Harvard Medical School, an author, and past president of the American Society for Microbiology. [1] [2] Kolter has been a professor at Harvard Medical School since 1983 and was Co-director of Harvard's Microbial Sciences Initiative from 2003-2018. [3] During the 35-year term of the Kolter laboratory from 1983 to 2018, more than 130 graduate students and postdoctoral trainees explored an eclectic mix of topics gravitating around the study of microbes. [4] [5] Kolter is a fellow of the American Association for the Advancement of Science and of the American Academy of Microbiology. [6]

Contents

As Professor Emeritus, Kolter has continued his involvement in science by communicating microbiology to scientific and general audiences. [7] [8] Since 2016, Kolter has been co-blogger (with Moselio Schaechter) of the popular microbiology blog, Small Things Considered . [9] From 2014 to 2018, Kolter and Scott Chimileski developed two exhibitions at the Harvard Museum of Natural History: World in a Drop, open in 2017, and Microbial Life , open through 2020. [10] In parallel, Chimileski and Kolter wrote the book Life at the Edge of Sight: A Photographic Exploration of the Microbial World (Harvard University Press, 2017). [7] [11] [12] During a 2018 interview at EAFIT University in Colombia, Kolter explained that he is “in a more contemplative phase of his career," adding that he is enjoying "being able to exercise a little more the 'Ph' (Philosophy) of my PhD". [8]

Early life, education and academic career

Kolter was born and raised in Guatemala. [9] He received a Bachelor of Science degree in Biology from Carnegie Mellon University in 1975 and a PhD in Biology from the University of California, San Diego in 1979. [7] He was then a Helen Hay Whitney Postdoctoral Fellow at Stanford University with Charles Yanofsky from 1980 to 1983. [7] Kolter joined the faculty at Harvard Medical School as an Assistant Professor in 1983, was promoted to Associate Professor in 1989, Professor in 1994, and became Professor Emeritus upon his retirement from running a research laboratory in 2018. [7]

Research

Summary

The research activities of Kolter's laboratory at Harvard Medical School from 1983 to 2018 encompassed several major parallel lines of investigation and spanned many interrelated subfields of microbiology. [5] [7] The overarching theme of the laboratory was to use genetic approaches to study physiological processes (and associated emergent properties) that bacteria have evolved to respond to stressful conditions in the environment, like starvation or limited nutrients, or as a result of ecological interactions with other living organisms. [7] [13] The eclectic nature of Kolter's research program was also a result of his policy of encouraging postdoctoral scientists to explore independent interests. [5] In an interview with Nature in 2015, Kolter was quoted on this mentorship style: "I let postdocs explore what they want to explore, as long as it is within the sphere of my interest." [5]

In total, Kolter has co-authored over 250 research and other scholarly articles which together have been cited over 50,000 times. [7] [14] [15] Kolter's research group was influential in the study of bacterial transport systems known as ABC exporters, published some of the earliest examples of experimental evolution through investigations of the stationary phase of bacterial growth, [7] [16] [17] [18] and was foundational in genetic studies of bacteria adhered to surfaces (living within communities called biofilms). [19] [20] The lab popularized the concept of bacterial biofilm formation as developmental or multicellular microbial processes, [21] [22] [23] and pioneered genetic studies of cellular differentiation, signaling, [24] and division of labor in bacteria. [25] [26] [27] In addition, his group has worked on other aspects of bacterial physiology, [28] the domestication of lab strains of bacteria, [29] microbiome ecology, [30] [31] [32] [33] interactions between plants and bacteria, [34] [35] [36] bacterial respiration processes, [37] and bioactive compound discovery. [38] [39] [40] [41]

Some of Kolter's significant scientific contributions are categorized below in chronological order.

Major topics of investigation

Regulation of DNA replication

As a graduate student, Kolter's research provided early evidence for what was called the "replicon hypothesis," proposed by Jacob, Brenner and Cuzin in 1962. [42] His work defined an origin of DNA replication that led to the development of many suicide cloning vectors still in use today.

  • Kolter, R; Helinski, DR (1978). "Construction of plasmid R6K derivatives in vitro: characterization of the R6K replication region". Plasmid. 1 (4): 571–80. doi:10.1016/0147-619X(78)90014-8. PMID   372982.
  • Kolter, R; Inuzuka, M; Helinski, DR (Dec 1978). "Trans-complementation-dependent replication of a low molecular weight origin fragment from plasmid R6K". Cell. 15 (4): 1199–208. doi:10.1016/0092-8674(78)90046-6. PMID   728998. S2CID   20082813.
  • Kolter, R; Helinski, DR (1982). "Plasmid R6K DNA replication. II. Direct nucleotide sequence repeats are required for an active gamma-origin". J Mol Biol. 161 (1): 45–56. doi:10.1016/0022-2836(82)90277-7. PMID   6296394.

Peptide antibiotic biosynthesis and ABC exporters

As a new faculty member at Harvard Medical school in the 1980s, Kolter's research group made use of Escherichia coli as a model organism for understanding the molecular genetics of antibiotic biosynthesis. During the course of this work the group was among the first to characterize ABC exporters, today known to be one of the most important membrane protein systems that move molecules across the cell membrane.

Physiology and evolution during stationary phase

In the late 1980s, Kolter's research group became interested in bacteria living in the stationary phase of the growth cycle, a state more like the natural conditions that bacteria experience in environments outside of the laboratory. [43] The group discovered regulatory systems exclusive to cells in this non-growing state and found that mutants with greater fitness in stationary phase evolved and rapidly took over the cultures. [16] [17] [44] The Zambrano et al. paper in 1993 which published this finding was one of the earliest examples of evolution occurring in the laboratory, or experimental evolution. [18]

Bacterial biofilms

In the 1990s, Kolter's group began to focus on the regulation and genetic components of surface-associated communities of bacteria called biofilms. Before then, biofilms had been discovered and were studied in the context of biofouling and in engineering solutions to prevent biofouling, [45] [46] [47] but the genetics of biofilm formation was unexplored and most microbiologists did not view biofilm formation as a physiological process of bacterial cells. [48] [49] [50] The lab went on to discover major regulatory systems underpinning biofilm development [51] [52] and characterized key materials within the extracellular matrix of biofilms using model species like Pseudomonasaeruginosa, [53] [54] [55] Escherichia coli , [56] Vibrio cholerae , [57] [58] and Bacillus subtilis. [59] [60] [61] [62] Microbial biofilms have since become a major field of microbiology, recognized as a predominant lifestyle of microbes in nature, with relevance to medicine and infections caused by pathogenic bacteria. [63] [64]

Microbial intraspecies interactions, cell differentiation & division of labor

Another body of research stemmed from work on biofilms in the Kolter group in collaboration with the laboratory of Richard Losick: the discovery that subpopulations of different functional cell types develop within single-species biofilms of the bacterium Bacillus subtilis . Some cells were found to express genes for motility, others for sporulation, cannibalism, surfactant production or the secretion of extracellular matrix. [26] Some cell types were found localized in clusters in different physical locations and time points during biofilm development. [25] Another study from the group in 2015 showed that collective behaviors like group migration across a surface can emerge due to interactions between multiple cell types. [27]

Microbial interspecies interactions

Much of Kolter's most recent work focused on interactions between several species in mixed communities, as they typically exist in natural environments. This work has produced several influential studies of the emergent properties and social behaviors of microbes while interacting with other species.

Communication of microbial science to the public

Kolter is an advocate and participant in the communication of microbial science to early career microbiologists and non-scientific audiences. [7] His work in this area began during his term as Co-Director of the Harvard Microbial Sciences Initiative from 2003 to 2018. In this role, Kolter organized an annual public lecture in Cambridge, Massachusetts on topics of general relevance, such as microbial foods and drinks like cheese, sake and wine. [65] His work in science communication then intensified in the years leading up to his retirement and now as an Emeritus professor through invited lectures, writing and museum projects. [8] [66]

Books

Museum exhibitions

From 2014 through 2018, Kolter and Scott Chimileski spearheaded two public exhibitions at the Harvard Museum of Natural History. [7] [11] World in a Drop: Photographic Explorations of Microbial Life was an artistic exhibition that featured imagery produced through Chimileski and Kolter's collaboration, and was open from August 2017 to January 2018. [67] Subsequently, Microbial Life: A Universe at the Edge of Sight opened in February 2018 as major special exhibition supported by the Alfred P. Sloan Foundation. Kolter and Chimileski are guest curators of Microbial Life and the exhibition remains open until March 2020. [10] These exhibitions have traveled internationally at the Eden Project in the UK and EAFIT University in Medellín, Colombia, among other locations. [7] [8] [68] [69] [70]

Chimileski and Kolter were also advisors and contributed imagery for Invisible Worlds at the Eden Project, a permanent exhibition sponsored by the Welcome Trust. [71] Their still and time-lapse imagery was featured in the Bacterial World Exhibition at the Oxford University Museum of Natural History in 2018, and in the World Unseen: Intersections of Art and Science at the David J. Sencer CDC Museum in Atlanta, Georgia in 2019.

Teaching and editing

Kolter has a long record of teaching at Harvard University and at international summer courses. At Harvard he taught Biofilm Dynamics and he is currently developing a Massive Open Online Course with HarvardX on fermentation and microbial foods. [72] He is a regular instructor at the Microbial Diversity Course at the Marine Biological Laboratory in Woods Hole, Massachusetts, the EMBO-FEBES summer microbiology course in Spetses, Greece and the John Innes/Rudjer Bošković Summer School in Applied Molecular Microbiology in Dubrovnik, Croatia. [7] In 2000, he received the ASM International Professorship Award. [7]

Kolter has been the cover editor of the Journal of Bacteriology since 1999 and was previously on the Board of Reviewing Editors for Science, mBio, and eLife. [7] [73]

Sources

  1. ↑ "Presidents of the Society (1899-present)". www.asm.org. Archived from the original on 2016-12-20. Retrieved 2017-07-24.
  2. ↑ "Department of Microbiology and Immunobiology | Faculty | Roberto Kolter, Ph.D." micro.med.harvard.edu. Retrieved 2017-07-21.
  3. ↑ "The Undiscovered Planet". Harvard Magazine. 2007-11-01. Retrieved 2017-07-22.
  4. ↑ "Kolter Lab | Unearthing the Secrets of the Microbial World | Harvard Medical School". gasp.med.harvard.edu. Retrieved 2017-07-21.
  5. 1 2 3 4 Gould, Julie (2015-05-28). "Turning point: Roberto Kolter". Nature. 521 (7553): 553. doi: 10.1038/nj7553-553a . ISSN   0028-0836. S2CID   177055203.
  6. ↑ "AAAS Members Elected as Fellows". AAAS - The World's Largest General Scientific Society. 2011-01-11. Archived from the original on 2018-09-13. Retrieved 2017-07-21.
  7. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 "The Kolter Lab | Roberto". gasp.med.harvard.edu. Retrieved 2019-07-30.
  8. 1 2 3 4 EAFIT, Universidad. "Solo mitad humanos". www.eafit.edu.co (in European Spanish). Retrieved 2019-07-30.
  9. 1 2 "Announcement". Small Things Considered. Retrieved 2017-07-21.
  10. 1 2 "At Harvard, microbes by the mile". Harvard Gazette. 2018-03-26. Retrieved 2019-07-30.
  11. 1 2 "Scott Chimileski Photography - Into the microbial world". www.scottchimileskiphotography.com. Retrieved 2019-07-30.
  12. ↑ Shaw, Jonathan (2017-08-03). "Life Beyond Sight". Harvard Magazine. Retrieved 2019-07-31.
  13. ↑ Rennie, John. "The Beautiful Intelligence of Bacteria and Other Microbes". Quanta Magazine. Retrieved 2019-07-31.
  14. ↑ "Roberto Kolter - Google Scholar Citations". scholar.google.com. Retrieved 2019-07-31.
  15. ↑ pubmeddev. "Kolter R - PubMed - NCBI". www.ncbi.nlm.nih.gov. Retrieved 2017-07-21.
  16. 1 2 Zambrano, M. M.; Siegele, D. A.; Almirón, M.; Tormo, A.; Kolter, R. (1993-03-19). "Microbial competition: Escherichia coli mutants that take over stationary phase cultures". Science. 259 (5102): 1757–1760. Bibcode:1993Sci...259.1757M. doi:10.1126/science.7681219. ISSN   0036-8075. PMID   7681219. S2CID   680360.
  17. 1 2 Kolter, Roberto; Finkel, Steven E. (1999-03-30). "Evolution of microbial diversity during prolonged starvation". Proceedings of the National Academy of Sciences. 96 (7): 4023–4027. Bibcode:1999PNAS...96.4023F. doi: 10.1073/pnas.96.7.4023 . ISSN   0027-8424. PMC   22413 . PMID   10097156.
  18. 1 2 Lenski, Richard E (October 2017). "Experimental evolution and the dynamics of adaptation and genome evolution in microbial populations". The ISME Journal. 11 (10): 2181–2194. Bibcode:2017ISMEJ..11.2181L. doi:10.1038/ismej.2017.69. ISSN   1751-7362. PMC   5607360 . PMID   28509909.
  19. ↑ "Signaling and Quorum Sensing". www.cs.montana.edu.
  20. ↑ O'Toole, George A.; Pratt, Leslie A.; Watnick, Paula I.; Newman, Dianne K.; Weaver, Valerie B.; Kolter, Roberto (1999-01-01). "[6] Genetic approaches to study of biofilms". Biofilms. Methods in Enzymology. Vol. 310. Academic Press. pp. 91–109. doi:10.1016/S0076-6879(99)10008-9. ISBN   9780121822118. PMID   10547784.
  21. ↑ Aguilar, Claudio; Vlamakis, Hera; Losick, Richard; Kolter, Roberto (December 2007). "Thinking about Bacillus subtilis as a multicellular organism". Current Opinion in Microbiology. 10 (6): 638–643. doi:10.1016/j.mib.2007.09.006. ISSN   1369-5274. PMC   2174258 . PMID   17977783.
  22. ↑ O'Toole, G.; Kaplan, H. B.; Kolter, R. (2000). "Biofilm formation as microbial development". Annual Review of Microbiology. 54: 49–79. doi:10.1146/annurev.micro.54.1.49. ISSN   0066-4227. PMID   11018124.
  23. ↑ Watnick, Paula; Kolter, Roberto (2000-05-15). "Biofilm, City of Microbes". Journal of Bacteriology. 182 (10): 2675–2679. doi:10.1128/JB.182.10.2675-2679.2000. ISSN   0021-9193. PMC   101960 . PMID   10781532.
  24. ↑ Romero, Diego; Traxler, Matthew F.; López, Daniel; Kolter, Roberto (2011-09-14). "Antibiotics as signal molecules". Chemical Reviews. 111 (9): 5492–5505. doi:10.1021/cr2000509. ISSN   1520-6890. PMC   3173521 . PMID   21786783.
  25. 1 2 Vlamakis, Hera; Aguilar, Claudio; Losick, Richard; Kolter, Roberto (2008-04-01). "Control of cell fate by the formation of an architecturally complex bacterial community". Genes & Development. 22 (7): 945–953. doi:10.1101/gad.1645008. ISSN   0890-9369. PMC   2279205 . PMID   18381896.
  26. 1 2 Lopez, Daniel; Vlamakis, Hera; Kolter, Roberto (January 2009). "Generation of multiple cell types in Bacillus subtilis". FEMS Microbiology Reviews. 33 (1): 152–163. doi: 10.1111/j.1574-6976.2008.00148.x . ISSN   0168-6445. PMID   19054118.
  27. 1 2 van Gestel, Jordi; Vlamakis, Hera; Kolter, Roberto (2015-04-20). "From Cell Differentiation to Cell Collectives: Bacillus subtilis Uses Division of Labor to Migrate". PLOS Biology. 13 (4): e1002141. doi: 10.1371/journal.pbio.1002141 . ISSN   1544-9173. PMC   4403855 . PMID   25894589.
  28. ↑ Finkel, S. E.; Kolter, R. (November 2001). "DNA as a nutrient: novel role for bacterial competence gene homologs". Journal of Bacteriology. 183 (21): 6288–6293. doi:10.1128/JB.183.21.6288-6293.2001. ISSN   0021-9193. PMC   100116 . PMID   11591672.
  29. ↑ McLoon, Anna L.; Guttenplan, Sarah B.; Kearns, Daniel B.; Kolter, Roberto; Losick, Richard (April 2011). "Tracing the domestication of a biofilm-forming bacterium". Journal of Bacteriology. 193 (8): 2027–2034. doi:10.1128/JB.01542-10. ISSN   1098-5530. PMC   3133032 . PMID   21278284.
  30. ↑ Lemon, Katherine P.; Klepac-Ceraj, Vanja; Schiffer, Hilary K.; Brodie, Eoin L.; Lynch, Susan V.; Kolter, Roberto (2010-06-22). "Comparative Analyses of the Bacterial Microbiota of the Human Nostril and Oropharynx". mBio. 1 (3). doi:10.1128/mBio.00129-10. ISSN   2150-7511. PMC   2925076 . PMID   20802827.
  31. ↑ Niu, Ben; Paulson, Joseph Nathaniel; Zheng, Xiaoqi; Kolter, Roberto (2017-03-21). "Simplified and representative bacterial community of maize roots". Proceedings of the National Academy of Sciences of the United States of America. 114 (12): E2450–E2459. Bibcode:2017PNAS..114E2450N. doi: 10.1073/pnas.1616148114 . ISSN   1091-6490. PMC   5373366 . PMID   28275097.
  32. ↑ Peterson, Celeste N.; Day, Stephanie; Wolfe, Benjamin E.; Ellison, Aaron M.; Kolter, Roberto; Pringle, Anne (September 2008). "A keystone predator controls bacterial diversity in the pitcher-plant (Sarracenia purpurea) microecosystem". Environmental Microbiology. 10 (9): 2257–2266. Bibcode:2008EnvMi..10.2257P. doi:10.1111/j.1462-2920.2008.01648.x. ISSN   1462-2920. PMID   18479443. S2CID   24215810.
  33. ↑ Gontang, Erin A.; Aylward, Frank O.; Carlos, Camila; Glavina del Rio, Tijana; Chovatia, Mansi; Fern, Alison; Lo, Chien-Chi; Malfatti, Stephanie A.; Tringe, Susannah G. (2017-05-18). "Major changes in microbial diversity and community composition across gut sections of a juvenile Panchlora cockroach". PLOS ONE. 12 (5): e0177189. Bibcode:2017PLoSO..1277189G. doi: 10.1371/journal.pone.0177189 . ISSN   1932-6203. PMC   5436645 . PMID   28545131.
  34. ↑ Chen, Yun; Cao, Shugeng; Chai, Yunrong; Clardy, Jon; Kolter, Roberto; Guo, Jian-hua; Losick, Richard (August 2012). "A Bacillus subtilis Sensor Kinase Involved in Triggering Biofilm Formation on the Roots of Tomato Plants". Molecular Microbiology. 85 (3): 418–430. doi:10.1111/j.1365-2958.2012.08109.x. ISSN   0950-382X. PMC   3518419 . PMID   22716461.
  35. ↑ Espinosa-Urgel, Manuel; Kolter, Roberto; Ramos, Juan-Luis (February 2002). "Root colonization by Pseudomonas putida: love at first sight". Microbiology. 148 (Pt 2): 341–343. doi: 10.1099/00221287-148-2-341 . ISSN   1350-0872. PMID   11832496. S2CID   42681037.
  36. ↑ Shapiro, Lori R.; Paulson, Joseph N.; Arnold, Brian J.; Scully, Erin D.; Zhaxybayeva, Olga; Pierce, Naomi E.; Rocha, Jorge; Klepac-Ceraj, Vanja; Holton, Kristina (October 2, 2018). "An Introduced Crop Plant Is Driving Diversification of the Virulent Bacterial Pathogen Erwinia tracheiphila". mBio. 9 (5). doi:10.1128/mBio.01307-18. ISSN   2150-7511. PMC   6168856 . PMID   30279283.
  37. ↑ Newman, D. K.; Kolter, R. (2000-05-04). "A role for excreted quinones in extracellular electron transfer". Nature. 405 (6782): 94–97. Bibcode:2000Natur.405...94N. doi:10.1038/35011098. ISSN   0028-0836. PMID   10811225. S2CID   4432099.
  38. ↑ "The Kolter Lab | Roberto Kolter". gasp.med.harvard.edu. Retrieved 2017-07-22.
  39. ↑ Kolter, Roberto; Clardy, Jon; Skaar, Eric P.; Koren, Sergey; Silva-Junior, Eduardo A.; Paludo, Camila R.; Horvath, Dennis J.; Ndousse-Fetter, Sula; Mevers, Emily (2018-10-02). "Amycomicin is a potent and specific antibiotic discovered with a targeted interaction screen". Proceedings of the National Academy of Sciences. 115 (40): 10124–10129. Bibcode:2018PNAS..11510124P. doi: 10.1073/pnas.1807613115 . ISSN   0027-8424. PMC   6176635 . PMID   30228116.
  40. ↑ Kolter, Roberto; van Wezel, Gilles P. (January 27, 2016). "Goodbye to brute force in antibiotic discovery?". Nature Microbiology. 1 (2): 15020. doi:10.1038/nmicrobiol.2015.20. hdl: 1887/3191938 . ISSN   2058-5276. PMID   27571977. S2CID   35052005.
  41. ↑ Seyedsayamdost, Mohammad R.; Traxler, Matthew F.; Clardy, Jon; Kolter, Roberto (2012). "Old meets new: using interspecies interactions to detect secondary metabolite production in actinomycetes". Natural Product Biosynthesis by Microorganisms and Plants, Part C. Methods in Enzymology. Vol. 517. pp. 89–109. doi:10.1016/B978-0-12-404634-4.00005-X. ISBN   9780124046344. ISSN   1557-7988. PMC   4004031 . PMID   23084935.
  42. ↑ Jacob, François; Brenner, Sydney; Cuzin, François (1963-01-01). "On the Regulation of DNA Replication in Bacteria". Cold Spring Harbor Symposia on Quantitative Biology. 28: 329–348. doi:10.1101/SQB.1963.028.01.048. ISSN   0091-7451.
  43. ↑ Connell, N.; Han, Z.; Moreno, F.; Kolter, R. (September 1987). "An E. coli promoter induced by the cessation of growth". Molecular Microbiology. 1 (2): 195–201. doi:10.1111/j.1365-2958.1987.tb00512.x. ISSN   0950-382X. PMID   2835580. S2CID   41850797.
  44. ↑ Zinser, E. R.; Kolter, R. (September 1999). "Mutations enhancing amino acid catabolism confer a growth advantage in stationary phase". Journal of Bacteriology. 181 (18): 5800–5807. doi:10.1128/jb.181.18.5800-5807.1999. ISSN   0021-9193. PMC   94102 . PMID   10482523.
  45. ↑ Henrici, Arthur T. (1933-03-01). "Studies of Freshwater Bacteria I. A Direct Microscopic Technique". Journal of Bacteriology. 25 (3): 277–287. doi:10.1128/JB.25.3.277-287.1933. ISSN   0021-9193. PMC   533461 . PMID   16559616.
  46. ↑ Zobell, Claude E. (1943). "The Effect of Solid Surfaces upon Bacterial Activity1". Journal of Bacteriology. 46 (1): 39–56. doi:10.1128/JB.46.1.39-56.1943. ISSN   0021-9193. PMC   373789 . PMID   16560677.
  47. ↑ Geesey, G. G.; Richardson, W. T.; Yeomans, H. G.; Irvin, R. T.; Costerton, J. W. (December 1977). "Microscopic examination of natural sessile bacterial populations from an alpine stream". Canadian Journal of Microbiology. 23 (12): 1733–1736. doi:10.1139/m77-249. ISSN   0008-4166. PMID   340020.
  48. ↑ Kolter, Roberto (March 2010). "Biofilms in lab and nature: a molecular geneticist's voyage to microbial ecology". International Microbiology. 13 (1): 1–7. doi:10.2436/20.1501.01.105. ISSN   1618-1905. PMID   20890834.
  49. ↑ Kolter, Roberto (2007-05-28). "Biology of Microbial Communities - Interview". Journal of Visualized Experiments (4): 205. doi:10.3791/205. ISSN   1940-087X. PMC   2556159 . PMID   18979009.
  50. ↑ O'Toole, George A. (2016-01-01). "Classic Spotlight: Before They Were Biofilms". Journal of Bacteriology. 198 (1): 5. doi:10.1128/JB.00593-15. ISSN   0021-9193. PMC   4686204 . PMID   26668270.
  51. ↑ Kearns, Daniel B.; Chu, Frances; Branda, Steven S.; Kolter, Roberto; Losick, Richard (February 2005). "A master regulator for biofilm formation by Bacillus subtilis". Molecular Microbiology. 55 (3): 739–749. doi: 10.1111/j.1365-2958.2004.04440.x . ISSN   0950-382X. PMID   15661000. S2CID   34300602.
  52. ↑ Branda, Steven S.; Vik, Shild; Friedman, Lisa; Kolter, Roberto (January 2005). "Biofilms: the matrix revisited". Trends in Microbiology. 13 (1): 20–26. doi:10.1016/j.tim.2004.11.006. ISSN   0966-842X. PMID   15639628.
  53. ↑ O'Toole, G. A.; Kolter, R. (October 1998). "Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development". Molecular Microbiology. 30 (2): 295–304. doi:10.1046/j.1365-2958.1998.01062.x. ISSN   0950-382X. PMID   9791175. S2CID   25140899.
  54. ↑ Sakuragi, Yumiko; Kolter, Roberto (July 2007). "Quorum-sensing regulation of the biofilm matrix genes (pel) of Pseudomonas aeruginosa". Journal of Bacteriology. 189 (14): 5383–5386. doi:10.1128/JB.00137-07. ISSN   0021-9193. PMC   1951888 . PMID   17496081.
  55. ↑ Friedman, Lisa; Kolter, Roberto (2004). "Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms". Molecular Microbiology. 51 (3): 675–690. doi:10.1046/j.1365-2958.2003.03877.x. ISSN   1365-2958. PMID   14731271. S2CID   20612916.
  56. ↑ Pratt, L. A.; Kolter, R. (October 1998). "Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili". Molecular Microbiology. 30 (2): 285–293. doi:10.1046/j.1365-2958.1998.01061.x. ISSN   0950-382X. PMID   9791174. S2CID   26631504.
  57. ↑ Watnick, P. I.; Kolter, R. (November 1999). "Steps in the development of a Vibrio cholerae El Tor biofilm". Molecular Microbiology. 34 (3): 586–595. doi:10.1046/j.1365-2958.1999.01624.x. ISSN   0950-382X. PMC   2860543 . PMID   10564499.
  58. ↑ Watnick, P. I.; Fullner, K. J.; Kolter, R. (June 1999). "A role for the mannose-sensitive hemagglutinin in biofilm formation by Vibrio cholerae El Tor". Journal of Bacteriology. 181 (11): 3606–3609. doi:10.1128/jb.181.11.3606-3609.1999. ISSN   0021-9193. PMC   93833 . PMID   10348878.
  59. ↑ Branda, Steven S.; González-Pastor, José Eduardo; Dervyn, Etienne; Ehrlich, S. Dusko; Losick, Richard; Kolter, Roberto (June 2004). "Genes involved in formation of structured multicellular communities by Bacillus subtilis". Journal of Bacteriology. 186 (12): 3970–3979. doi:10.1128/JB.186.12.3970-3979.2004. ISSN   0021-9193. PMC   419949 . PMID   15175311.
  60. ↑ Branda, Steven S.; Chu, Frances; Kearns, Daniel B.; Losick, Richard; Kolter, Roberto (February 2006). "A major protein component of the Bacillus subtilis biofilm matrix". Molecular Microbiology. 59 (4): 1229–1238. doi: 10.1111/j.1365-2958.2005.05020.x . ISSN   0950-382X. PMID   16430696. S2CID   3041295.
  61. ↑ Romero, Diego; Aguilar, Claudio; Losick, Richard; Kolter, Roberto (2010-02-02). "Amyloid fibers provide structural integrity to Bacillus subtilis biofilms". Proceedings of the National Academy of Sciences. 107 (5): 2230–2234. Bibcode:2010PNAS..107.2230R. doi: 10.1073/pnas.0910560107 . ISSN   0027-8424. PMC   2836674 . PMID   20080671.
  62. ↑ Science News, Dec. 22, 2008
  63. ↑ Hall-Stoodley, Luanne; Costerton, J. William; Stoodley, Paul (February 2004). "Bacterial biofilms: from the natural environment to infectious diseases". Nature Reviews. Microbiology. 2 (2): 95–108. doi:10.1038/nrmicro821. ISSN   1740-1526. PMID   15040259. S2CID   9107205.
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