Roberto Kolter

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 student 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]

Roberto Kolter
Born1953
Guatemala
Known forbiofilms, stationary phase, antibiotic biosynthesis
Scientific career
FieldsMicrobiology, Molecular genetics, Chemical ecology, Molecular microbiology, microbial ecology
InstitutionsHarvard Medical School
Doctoral advisorDonald Helinski
Other academic advisorsCharles Yanofsky
Websitehttp://gasp.med.harvard.edu/

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.

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 Pseudomonas aeruginosa,[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
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  16. 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. 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. 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. doi:10.1038/ismej.2017.69. ISSN 1751-7362. PMC 5607360. PMID 28509909.
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  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. Biofilms. 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. 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. 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. 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. 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. 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 (Reading, England). 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.
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  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. 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. 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". Methods in Enzymology. 517: 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.
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  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.
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  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.
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  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.
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