Roberto Kolter

{{short description|Microbiologist and teacher, born 1953}}

{{Infobox scientist

| name = Roberto Kolter

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| birth_place = Guatemala

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| fields = Microbiology, molecular genetics, chemical ecology, molecular microbiology,

microbial ecology

| workplaces = Harvard Medical School

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| doctoral_advisor = Donald Helinski

| academic_advisors = Charles Yanofsky

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| known_for = Biofilms, stationary phase, antibiotic biosynthesis

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| website = http://gasp.med.harvard.edu/

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| birth_date = 1953

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Roberto Kolter is professor of microbiology, emeritus, at Harvard Medical School, an author, and past president of the American Society for Microbiology.{{Cite web|url=https://www.asm.org/index.php/71-membership/archives/913-presidents-of-the-society|title=Presidents of the Society (1899-present)|website=www.asm.org|access-date=2017-07-24|archive-date=2016-12-20|archive-url=https://web.archive.org/web/20161220122434/http://www.asm.org/index.php/71-membership/archives/913-presidents-of-the-society|url-status=dead}}{{Cite web|url=http://micro.med.harvard.edu/faculty/kolter.html|title=Department of Microbiology and Immunobiology {{!}} Faculty {{!}} Roberto Kolter, Ph.D.|website=micro.med.harvard.edu|access-date=2017-07-21}} Kolter has been a professor at Harvard Medical School since 1983 and was Co-director of Harvard's Microbial Sciences Initiative from 2003-2018.{{Cite news|url=http://harvardmagazine.com/2007/11/the-undiscovered-planet.html|title=The Undiscovered Planet|date=2007-11-01|work=Harvard Magazine|access-date=2017-07-22}} 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.{{Cite web|url=http://gasp.med.harvard.edu/|title=Kolter Lab {{!}} Unearthing the Secrets of the Microbial World {{!}} Harvard Medical School|website=gasp.med.harvard.edu|access-date=2017-07-21}}{{Cite journal|last=Gould|first=Julie|date=2015-05-28|title=Turning point: Roberto Kolter|journal=Nature|volume=521|issue=7553|pages=553|doi=10.1038/nj7553-553a|s2cid=177055203 |issn=0028-0836|doi-access=free}} Kolter is a fellow of the American Association for the Advancement of Science and of the American Academy of Microbiology.{{Cite news|url=https://www.aaas.org/news/2011/01/11/aaas-members-elected-fellows|title=AAAS Members Elected as Fellows|date=2011-01-11|work=AAAS - The World's Largest General Scientific Society|access-date=2017-07-21|archive-date=2018-09-13|archive-url=https://web.archive.org/web/20180913040407/https://www.aaas.org/news/2011/01/11/aaas-members-elected-fellows|url-status=dead}}

As professor emeritus, Kolter has continued his involvement in science by communicating microbiology to scientific and general audiences.{{Cite web|url=http://www.eafit.edu.co:80/noticias/revistauniversidadeafit/173/solo-mitad-humanos|title=Solo mitad humanos|last=EAFIT|first=Universidad|website=www.eafit.edu.co|language=es-ES|access-date=2019-07-30}} Since 2016, Kolter has been co-blogger (with Moselio Schaechter) of the popular microbiology blog, [http://schaechter.asmblog.org/schaechter/ Small Things Considered].{{Cite web|url=http://schaechter.asmblog.org/schaechter/2016/10/announcement.html|title=Announcement|website=Small Things Considered|access-date=2017-07-21}} From 2014 to 2018, Kolter and Scott Chimileski developed two exhibitions at the Harvard Museum of Natural History: [https://hmnh.harvard.edu/world-drop-photographic-explorations-microbial-life World in a Drop], open in 2017, and [https://hmnh.harvard.edu/microbial-life-universe-edge-sight Microbial Life], open through 2020.{{Cite web|url=https://news.harvard.edu/gazette/story/2018/03/at-harvard-microbes-by-the-mile/|title=At Harvard, microbes by the mile|date=2018-03-26|website=Harvard Gazette|access-date=2019-07-30}} In parallel, Chimileski and Kolter wrote the book [http://www.hup.harvard.edu/catalog.php?isbn=9780674975910 Life at the Edge of Sight: A Photographic Exploration of the Microbial World] (Harvard University Press, 2017).{{Cite web|url=https://www.scottchimileskiphotography.com/|title=Scott Chimileski Photography - Into the microbial world|website=www.scottchimileskiphotography.com|access-date=2019-07-30}}{{Cite web|url=https://harvardmagazine.com/2017/09/microbes-in-soil|title=Life Beyond Sight|last=Shaw|first=Jonathan|date=2017-08-03|website=Harvard Magazine|access-date=2019-07-31}} During a 2018 [http://www.eafit.edu.co/noticias/revistauniversidadeafit/173/solo-mitad-humanos 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".

Early life, education and academic career

Kolter was born and raised in Guatemala. 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. He was then a Helen Hay Whitney Postdoctoral Fellow at Stanford University with Charles Yanofsky from 1980 to 1983. 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.

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. 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.{{Cite web|url=https://www.quantamagazine.org/the-beautiful-intelligence-of-bacteria-and-other-microbes-20171113/|title=The Beautiful Intelligence of Bacteria and Other Microbes|last=Rennie|first=John|website=Quanta Magazine|access-date=2019-07-31}} The eclectic nature of Kolter's research program was also a result of his policy of encouraging postdoctoral scientists to explore independent interests. 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."

In total, Kolter has co-authored over 250 research and other scholarly articles which together have been cited over 50,000 times.{{Cite web|url=https://scholar.google.com/citations?user=yW9RJEQAAAAJ&hl=en&oi=ao|title=Roberto Kolter - Google Scholar Citations|website=scholar.google.com|access-date=2019-07-31}}{{Cite web|url=https://www.ncbi.nlm.nih.gov/pubmed?dispmax=20&pmfilter_EDatLimit=added+to+PubMed+in+the+last+5+years&cmd_current=Limits&orig_db=PubMed&cmd=Search&term=Kolter+R&doptcmdl=DocSum|title=Kolter R - PubMed - NCBI|last=pubmeddev|website=www.ncbi.nlm.nih.gov|access-date=2017-07-21}} 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,{{Cite web|url=http://gasp.med.harvard.edu/research/research.html|title=The Kolter Lab {{!}} Roberto|website=gasp.med.harvard.edu|access-date=2019-07-30}}{{Cite journal|last1=Zambrano|first1=M. M.|last2=Siegele|first2=D. A.|last3=Almirón|first3=M.|last4=Tormo|first4=A.|last5=Kolter|first5=R.|date=1993-03-19|title=Microbial competition: Escherichia coli mutants that take over stationary phase cultures|journal=Science|volume=259|issue=5102|pages=1757–1760|doi=10.1126/science.7681219|issn=0036-8075|pmid=7681219|bibcode=1993Sci...259.1757M|s2cid=680360|url=https://semanticscholar.org/paper/218937d2c8f65ab61888a700e7bf89763f69b138}}{{Cite journal|last1=Kolter|first1=Roberto|last2=Finkel|first2=Steven E.|date=1999-03-30|title=Evolution of microbial diversity during prolonged starvation|journal=Proceedings of the National Academy of Sciences|volume=96|issue=7|pages=4023–4027|doi=10.1073/pnas.96.7.4023|issn=0027-8424|pmid=10097156|pmc=22413|bibcode=1999PNAS...96.4023F|doi-access=free}} and was foundational in genetic studies of bacteria adhered to surfaces (living within communities called biofilms).{{Cite web|url=https://www.cs.montana.edu/webworks/projects/stevesbook/contents/chapters/chapter002/section005/blue/page002.html|title=Signaling and Quorum Sensing|website=www.cs.montana.edu}}{{cite book|last1=O'Toole|first1=George A.|chapter=[6] Genetic approaches to study of biofilms|date=1999-01-01|series=Methods in Enzymology|volume=310|pages=91–109|publisher=Academic Press|last2=Pratt|first2=Leslie A.|last3=Watnick|first3=Paula I.|last4=Newman|first4=Dianne K.|last5=Weaver|first5=Valerie B.|last6=Kolter|first6=Roberto|doi=10.1016/S0076-6879(99)10008-9|pmid=10547784|title=Biofilms|isbn=9780121822118}} The lab popularized the concept of bacterial biofilm formation as developmental or multicellular microbial processes,{{Cite journal|last1=Aguilar|first1=Claudio|last2=Vlamakis|first2=Hera|last3=Losick|first3=Richard|last4=Kolter|first4=Roberto|date=December 2007|title=Thinking about Bacillus subtilis as a multicellular organism|journal=Current Opinion in Microbiology|volume=10|issue=6|pages=638–643|doi=10.1016/j.mib.2007.09.006|issn=1369-5274|pmc=2174258|pmid=17977783}}{{Cite journal|last1=O'Toole|first1=G.|last2=Kaplan|first2=H. B.|last3=Kolter|first3=R.|date=2000|title=Biofilm formation as microbial development|journal=Annual Review of Microbiology|volume=54|pages=49–79|doi=10.1146/annurev.micro.54.1.49|issn=0066-4227|pmid=11018124}}{{Cite journal|last1=Watnick|first1=Paula|last2=Kolter|first2=Roberto|date=2000-05-15|title=Biofilm, City of Microbes|journal=Journal of Bacteriology|volume=182|issue=10|pages=2675–2679|doi=10.1128/JB.182.10.2675-2679.2000|issn=0021-9193|pmid=10781532|pmc=101960}} and pioneered genetic studies of cellular differentiation, signaling,{{Cite journal|last1=Romero|first1=Diego|last2=Traxler|first2=Matthew F.|last3=López|first3=Daniel|last4=Kolter|first4=Roberto|date=2011-09-14|title=Antibiotics as signal molecules|journal=Chemical Reviews|volume=111|issue=9|pages=5492–5505|doi=10.1021/cr2000509|issn=1520-6890|pmc=3173521|pmid=21786783}} and division of labor in bacteria.{{Cite journal|last1=Vlamakis|first1=Hera|last2=Aguilar|first2=Claudio|last3=Losick|first3=Richard|last4=Kolter|first4=Roberto|date=2008-04-01|title=Control of cell fate by the formation of an architecturally complex bacterial community|journal=Genes & Development|volume=22|issue=7|pages=945–953|doi=10.1101/gad.1645008|issn=0890-9369|pmc=2279205|pmid=18381896}}{{Cite journal|last1=Lopez|first1=Daniel|last2=Vlamakis|first2=Hera|last3=Kolter|first3=Roberto|date=January 2009|title=Generation of multiple cell types in Bacillus subtilis|journal=FEMS Microbiology Reviews|volume=33|issue=1|pages=152–163|doi=10.1111/j.1574-6976.2008.00148.x|issn=0168-6445|pmid=19054118|doi-access=free}}{{Cite journal|last1=van Gestel|first1=Jordi|last2=Vlamakis|first2=Hera|last3=Kolter|first3=Roberto|date=2015-04-20|title=From Cell Differentiation to Cell Collectives: Bacillus subtilis Uses Division of Labor to Migrate|journal=PLOS Biology|volume=13|issue=4|doi=10.1371/journal.pbio.1002141|issn=1544-9173|pmc=4403855|pmid=25894589|page=e1002141 |doi-access=free }} In addition, his group has worked on other aspects of bacterial physiology,{{Cite journal|last1=Finkel|first1=S. E.|last2=Kolter|first2=R.|date=November 2001|title=DNA as a nutrient: novel role for bacterial competence gene homologs|journal=Journal of Bacteriology|volume=183|issue=21|pages=6288–6293|doi=10.1128/JB.183.21.6288-6293.2001|issn=0021-9193|pmid=11591672|pmc=100116}} the domestication of lab strains of bacteria,{{Cite journal|last1=McLoon|first1=Anna L.|last2=Guttenplan|first2=Sarah B.|last3=Kearns|first3=Daniel B.|last4=Kolter|first4=Roberto|last5=Losick|first5=Richard|date=April 2011|title=Tracing the domestication of a biofilm-forming bacterium|journal=Journal of Bacteriology|volume=193|issue=8|pages=2027–2034|doi=10.1128/JB.01542-10|issn=1098-5530|pmc=3133032|pmid=21278284}} microbiome ecology,{{Cite journal|last1=Lemon|first1=Katherine P.|last2=Klepac-Ceraj|first2=Vanja|last3=Schiffer|first3=Hilary K.|last4=Brodie|first4=Eoin L.|last5=Lynch|first5=Susan V.|last6=Kolter|first6=Roberto|date=2010-06-22|title=Comparative Analyses of the Bacterial Microbiota of the Human Nostril and Oropharynx|journal=mBio|volume=1|issue=3|doi=10.1128/mBio.00129-10|issn=2150-7511|pmc=2925076|pmid=20802827}}{{Cite journal|last1=Niu|first1=Ben|last2=Paulson|first2=Joseph Nathaniel|last3=Zheng|first3=Xiaoqi|last4=Kolter|first4=Roberto|date=2017-03-21|title=Simplified and representative bacterial community of maize roots|journal=Proceedings of the National Academy of Sciences of the United States of America|volume=114|issue=12|pages=E2450–E2459|doi=10.1073/pnas.1616148114|issn=1091-6490|pmc=5373366|pmid=28275097|doi-access=free|bibcode=2017PNAS..114E2450N }}{{Cite journal|last1=Peterson|first1=Celeste N.|last2=Day|first2=Stephanie|last3=Wolfe|first3=Benjamin E.|last4=Ellison|first4=Aaron M.|last5=Kolter|first5=Roberto|last6=Pringle|first6=Anne|date=September 2008|title=A keystone predator controls bacterial diversity in the pitcher-plant (Sarracenia purpurea) microecosystem|journal=Environmental Microbiology|volume=10|issue=9|pages=2257–2266|doi=10.1111/j.1462-2920.2008.01648.x|issn=1462-2920|pmid=18479443|bibcode=2008EnvMi..10.2257P |s2cid=24215810}}{{Cite journal|last1=Gontang|first1=Erin A.|last2=Aylward|first2=Frank O.|last3=Carlos|first3=Camila|last4=Glavina del Rio|first4=Tijana|last5=Chovatia|first5=Mansi|last6=Fern|first6=Alison|last7=Lo|first7=Chien-Chi|last8=Malfatti|first8=Stephanie A.|last9=Tringe|first9=Susannah G.|date=2017-05-18|title=Major changes in microbial diversity and community composition across gut sections of a juvenile Panchlora cockroach|journal=PLOS ONE|volume=12|issue=5|pages=e0177189|doi=10.1371/journal.pone.0177189|issn=1932-6203|pmc=5436645|pmid=28545131|bibcode=2017PLoSO..1277189G|doi-access=free}} interactions between plants and bacteria,{{Cite journal|last1=Chen|first1=Yun|last2=Cao|first2=Shugeng|last3=Chai|first3=Yunrong|last4=Clardy|first4=Jon|last5=Kolter|first5=Roberto|last6=Guo|first6=Jian-hua|last7=Losick|first7=Richard|date=August 2012|title=A Bacillus subtilis Sensor Kinase Involved in Triggering Biofilm Formation on the Roots of Tomato Plants|journal=Molecular Microbiology|volume=85|issue=3|pages=418–430|doi=10.1111/j.1365-2958.2012.08109.x|issn=0950-382X|pmc=3518419|pmid=22716461}}{{Cite journal|last1=Espinosa-Urgel|first1=Manuel|last2=Kolter|first2=Roberto|last3=Ramos|first3=Juan-Luis|date=February 2002|title=Root colonization by Pseudomonas putida: love at first sight|journal=Microbiology |volume=148|issue=Pt 2|pages=341–343|doi=10.1099/00221287-148-2-341|issn=1350-0872|pmid=11832496|s2cid=42681037|doi-access=free}}{{Cite journal|last1=Shapiro|first1=Lori R.|last2=Paulson|first2=Joseph N.|last3=Arnold|first3=Brian J.|last4=Scully|first4=Erin D.|last5=Zhaxybayeva|first5=Olga|last6=Pierce|first6=Naomi E.|last7=Rocha|first7=Jorge|last8=Klepac-Ceraj|first8=Vanja|last9=Holton|first9=Kristina|date=October 2, 2018|title=An Introduced Crop Plant Is Driving Diversification of the Virulent Bacterial Pathogen Erwinia tracheiphila|journal=mBio|volume=9|issue=5|doi=10.1128/mBio.01307-18|issn=2150-7511|pmc=6168856|pmid=30279283}} bacterial respiration processes,{{Cite journal|last1=Newman|first1=D. K.|last2=Kolter|first2=R.|date=2000-05-04|title=A role for excreted quinones in extracellular electron transfer|journal=Nature|volume=405|issue=6782|pages=94–97|doi=10.1038/35011098|issn=0028-0836|pmid=10811225|bibcode=2000Natur.405...94N|s2cid=4432099}} and bioactive compound discovery.{{Cite web|url=http://gasp.med.harvard.edu/members/rkolter.html|title=The Kolter Lab {{!}} Roberto Kolter|website=gasp.med.harvard.edu|access-date=2017-07-22}}{{Cite journal|last1=Kolter|first1=Roberto|last2=Clardy|first2=Jon|last3=Skaar|first3=Eric P.|last4=Koren|first4=Sergey|last5=Silva-Junior|first5=Eduardo A.|last6=Paludo|first6=Camila R.|last7=Horvath|first7=Dennis J.|last8=Ndousse-Fetter|first8=Sula|last9=Mevers|first9=Emily|date=2018-10-02|title=Amycomicin is a potent and specific antibiotic discovered with a targeted interaction screen|journal=Proceedings of the National Academy of Sciences|volume=115|issue=40|pages=10124–10129|doi=10.1073/pnas.1807613115|issn=0027-8424|pmid=30228116|pmc=6176635|doi-access=free|bibcode=2018PNAS..11510124P }}{{Cite journal|last1=Kolter|first1=Roberto|last2=van Wezel|first2=Gilles P.|date=January 27, 2016|title=Goodbye to brute force in antibiotic discovery?|journal=Nature Microbiology|volume=1|issue=2|pages=15020|doi=10.1038/nmicrobiol.2015.20|issn=2058-5276|pmid=27571977|hdl=1887/3191938|s2cid=35052005|hdl-access=free}}{{Cite book|last1=Seyedsayamdost|first1=Mohammad R.|last2=Traxler|first2=Matthew F.|last3=Clardy|first3=Jon|last4=Kolter|first4=Roberto|title=Natural Product Biosynthesis by Microorganisms and Plants, Part C |date=2012|chapter=Old meets new: using interspecies interactions to detect secondary metabolite production in actinomycetes|series=Methods in Enzymology|volume=517|pages=89–109|doi=10.1016/B978-0-12-404634-4.00005-X|issn=1557-7988|pmc=4004031|pmid=23084935|isbn=9780124046344}}

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.{{Cite journal|last1=Jacob|first1=François|last2=Brenner|first2=Sydney|last3=Cuzin|first3=François|date=1963-01-01|title=On the Regulation of DNA Replication in Bacteria|journal=Cold Spring Harbor Symposia on Quantitative Biology|volume=28|pages=329–348|doi=10.1101/SQB.1963.028.01.048|issn=0091-7451}} His work defined an origin of DNA replication that led to the development of many suicide cloning vectors still in use today.

  • {{cite journal | last1 = Kolter | first1 = R | last2 = Helinski | first2 = DR | year = 1978 | title = Construction of plasmid R6K derivatives in vitro: characterization of the R6K replication region | journal = Plasmid | volume = 1 | issue = 4| pages = 571–80 | doi = 10.1016/0147-619X(78)90014-8 | pmid = 372982 }}
  • {{cite journal | last1 = Kolter | first1 = R | last2 = Inuzuka | first2 = M | last3 = Helinski | first3 = DR | date = Dec 1978 | title = Trans-complementation-dependent replication of a low molecular weight origin fragment from plasmid R6K | journal = Cell | volume = 15 | issue = 4| pages = 1199–208 | pmid = 728998 | doi = 10.1016/0092-8674(78)90046-6 | s2cid = 20082813 }}
  • {{cite journal | last1 = Kolter | first1 = R | last2 = Helinski | first2 = DR | year = 1982 | title = Plasmid R6K DNA replication. II. Direct nucleotide sequence repeats are required for an active gamma-origin | journal = J Mol Biol | volume = 161 | issue = 1| pages = 45–56 | pmid = 6296394 | doi = 10.1016/0022-2836(82)90277-7 }}

== 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.

  • {{cite journal | last1 = Gilson | first1 = L | last2 = Mahanty | first2 = HK | last3 = Kolter | first3 = R | year = 1990 | title = Genetic analysis of an MDR-like export system: the secretion of colicin V | journal = EMBO J. | volume = 9 | issue = 12| pages = 3875–84 | pmid = 2249654 | pmc = 552155 | doi = 10.1002/j.1460-2075.1990.tb07606.x }}
  • {{cite journal | last1 = Fath | first1 = MJ | last2 = Kolter | first2 = R | year = 1993 | title = ABC transporters: bacterial exporters | journal = Microbiol. Rev. | volume = 57 | issue = 4| pages = 995–1017 | pmid = 8302219 | pmc = 372944 | doi = 10.1128/mmbr.57.4.995-1017.1993 }}
  • {{cite journal | last1 = Yorgey | first1 = P | last2 = Lee | first2 = J | last3 = Kördel | first3 = J | last4 = Vivas | first4 = E | last5 = Warner | first5 = P | last6 = Jebaratnam | first6 = D | last7 = Kolter | first7 = R | year = 1994 | title = Posttranslational modifications in microcin B17 define an additional class of DNA gyrase inhibitor | journal = Proc Natl Acad Sci U S A | volume = 91 | issue = 10| pages = 4519–23 | pmc = 43817 | pmid = 8183941 | doi = 10.1073/pnas.91.10.4519 | bibcode = 1994PNAS...91.4519Y | doi-access = free }}

== 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.{{Cite journal|last1=Connell|first1=N.|last2=Han|first2=Z.|last3=Moreno|first3=F.|last4=Kolter|first4=R.|date=September 1987|title=An E. coli promoter induced by the cessation of growth|journal=Molecular Microbiology|volume=1|issue=2|pages=195–201|doi=10.1111/j.1365-2958.1987.tb00512.x|issn=0950-382X|pmid=2835580|s2cid=41850797}} 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.{{Cite journal|last1=Zinser|first1=E. R.|last2=Kolter|first2=R.|date=September 1999|title=Mutations enhancing amino acid catabolism confer a growth advantage in stationary phase|journal=Journal of Bacteriology|volume=181|issue=18|pages=5800–5807|issn=0021-9193|pmid=10482523|pmc=94102|doi=10.1128/jb.181.18.5800-5807.1999}} 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.{{Cite journal|last=Lenski|first=Richard E|date=October 2017|title=Experimental evolution and the dynamics of adaptation and genome evolution in microbial populations|journal=The ISME Journal|volume=11|issue=10|pages=2181–2194|doi=10.1038/ismej.2017.69|issn=1751-7362|pmc=5607360|pmid=28509909|bibcode=2017ISMEJ..11.2181L }}

  • {{cite journal | last1 = Almirón | first1 = M | last2 = Link | first2 = AJ | last3 = Furlong | first3 = D | last4 = Kolter | year = 1992 | title = Escherichia coli | journal = Genes Dev | volume = 6 | issue = 12B| pages = 2646–54 | pmid = 1340475 | doi = 10.1101/gad.6.12b.2646 | s2cid = 10308477 | doi-access = free }}
  • {{cite journal | last1 = Siegele | first1 = D | last2 = Kolter | first2 = R | year = 1992 | title = Life after log | journal = J Bacteriol | volume = 174 | issue = 2| pages = 345–348 | pmc = 205722 | pmid = 1729229 | doi = 10.1128/jb.174.2.345-348.1992 }}
  • {{cite journal | last1 = Zambrano | first1 = MM | last2 = Siegele | first2 = DA | last3 = Almirón | first3 = M | last4 = Tormo | first4 = A | last5 = Kolter | year = 1993 | title = Escherichia coli mutants that take over stationary phase cultures | url = https://semanticscholar.org/paper/218937d2c8f65ab61888a700e7bf89763f69b138| journal = Science | volume = 259 | issue = 5102| pages = 1757–60 | pmid = 7681219 | doi = 10.1126/science.7681219 | bibcode = 1993Sci...259.1757M | s2cid = 680360 }}
  • {{cite journal | last1 = Kolter | first1 = R | last2 = Siegele | first2 = DA | last3 = Tormo | first3 = A | year = 1993 | title = The stationary phase of the bacterial life cycle | journal = Annu Rev Microbiol | volume = 47 | pages = 855–74 | pmid = 8257118 | doi = 10.1146/annurev.mi.47.100193.004231 }}
  • {{cite journal | last1 = Zambrano | first1 = MM | last2 = Kolter | first2 = R | year = 1996 | title = GASPing for life in stationary phase | journal = Cell | volume = 86 | issue = 2| pages = 181–4 | pmid = 8706122 | doi = 10.1016/s0092-8674(00)80089-6 | s2cid = 13569021 | doi-access = free }}

== 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,{{Cite journal|last=Henrici|first=Arthur T.|date=1933-03-01|title=Studies of Freshwater Bacteria I. A Direct Microscopic Technique|journal=Journal of Bacteriology|volume=25|issue=3|pages=277–287|issn=0021-9193|pmc=533461|pmid=16559616|doi=10.1128/JB.25.3.277-287.1933}}{{Cite journal|last=Zobell|first=Claude E.|date=1943|title=The Effect of Solid Surfaces upon Bacterial Activity1|journal=Journal of Bacteriology|volume=46|issue=1|pages=39–56|issn=0021-9193|pmc=373789|pmid=16560677|doi=10.1128/JB.46.1.39-56.1943}}{{Cite journal|last1=Geesey|first1=G. G.|last2=Richardson|first2=W. T.|last3=Yeomans|first3=H. G.|last4=Irvin|first4=R. T.|last5=Costerton|first5=J. W.|date=December 1977|title=Microscopic examination of natural sessile bacterial populations from an alpine stream|journal=Canadian Journal of Microbiology|volume=23|issue=12|pages=1733–1736|issn=0008-4166|pmid=340020|doi=10.1139/m77-249}} but the genetics of biofilm formation was unexplored and most microbiologists did not view biofilm formation as a physiological process of bacterial cells.{{Cite journal|last=Kolter|first=Roberto|date=March 2010|title=Biofilms in lab and nature: a molecular geneticist's voyage to microbial ecology|journal=International Microbiology|volume=13|issue=1|pages=1–7|doi=10.2436/20.1501.01.105|issn=1618-1905|pmid=20890834}}{{Cite journal|last=Kolter|first=Roberto|date=2007-05-28|title=Biology of Microbial Communities - Interview|url=https://www.jove.com/video/205/biology-of-microbial-communities-interview|journal=Journal of Visualized Experiments|issue=4|doi=10.3791/205|issn=1940-087X|pmc=2556159|pmid=18979009|page=205}}{{Cite journal|last=O'Toole|first=George A.|date=2016-01-01|title=Classic Spotlight: Before They Were Biofilms|journal=Journal of Bacteriology|volume=198|issue=1|pages=5|doi=10.1128/JB.00593-15|issn=0021-9193|pmc=4686204|pmid=26668270}} The lab went on to discover major regulatory systems underpinning biofilm development{{Cite journal|last1=Kearns|first1=Daniel B.|last2=Chu|first2=Frances|last3=Branda|first3=Steven S.|last4=Kolter|first4=Roberto|last5=Losick|first5=Richard|date=February 2005|title=A master regulator for biofilm formation by Bacillus subtilis|journal=Molecular Microbiology|volume=55|issue=3|pages=739–749|doi=10.1111/j.1365-2958.2004.04440.x|issn=0950-382X|pmid=15661000|s2cid=34300602|doi-access=free}}{{Cite journal|last1=Branda|first1=Steven S.|last2=Vik|first2=Shild|last3=Friedman|first3=Lisa|last4=Kolter|first4=Roberto|date=January 2005|title=Biofilms: the matrix revisited|journal=Trends in Microbiology|volume=13|issue=1|pages=20–26|doi=10.1016/j.tim.2004.11.006|issn=0966-842X|pmid=15639628}} and characterized key materials within the extracellular matrix of biofilms using model species like Pseudomonas aeruginosa,{{Cite journal|last1=O'Toole|first1=G. A.|last2=Kolter|first2=R.|date=October 1998|title=Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development|journal=Molecular Microbiology|volume=30|issue=2|pages=295–304|doi=10.1046/j.1365-2958.1998.01062.x|issn=0950-382X|pmid=9791175|s2cid=25140899}}{{Cite journal|last1=Sakuragi|first1=Yumiko|last2=Kolter|first2=Roberto|date=July 2007|title=Quorum-sensing regulation of the biofilm matrix genes (pel) of Pseudomonas aeruginosa|journal=Journal of Bacteriology|volume=189|issue=14|pages=5383–5386|doi=10.1128/JB.00137-07|issn=0021-9193|pmc=1951888|pmid=17496081}}{{Cite journal|last1=Friedman|first1=Lisa|last2=Kolter|first2=Roberto|date=2004|title=Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms|journal=Molecular Microbiology|volume=51|issue=3|pages=675–690|doi=10.1046/j.1365-2958.2003.03877.x|pmid=14731271|s2cid=20612916|issn=1365-2958}} Escherichia coli,{{Cite journal|last1=Pratt|first1=L. A.|last2=Kolter|first2=R.|date=October 1998|title=Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili|journal=Molecular Microbiology|volume=30|issue=2|pages=285–293|doi=10.1046/j.1365-2958.1998.01061.x|issn=0950-382X|pmid=9791174|s2cid=26631504}} Vibrio cholerae,{{Cite journal|last1=Watnick|first1=P. I.|last2=Kolter|first2=R.|date=November 1999|title=Steps in the development of a Vibrio cholerae El Tor biofilm|journal=Molecular Microbiology|volume=34|issue=3|pages=586–595|doi=10.1046/j.1365-2958.1999.01624.x|issn=0950-382X|pmc=2860543|pmid=10564499}}{{Cite journal|last1=Watnick|first1=P. I.|last2=Fullner|first2=K. J.|last3=Kolter|first3=R.|date=June 1999|title=A role for the mannose-sensitive hemagglutinin in biofilm formation by Vibrio cholerae El Tor|journal=Journal of Bacteriology|volume=181|issue=11|pages=3606–3609|issn=0021-9193|pmid=10348878|pmc=93833|doi=10.1128/jb.181.11.3606-3609.1999}} and Bacillus subtilis.{{Cite journal|last1=Branda|first1=Steven S.|last2=González-Pastor|first2=José Eduardo|last3=Dervyn|first3=Etienne|last4=Ehrlich|first4=S. Dusko|last5=Losick|first5=Richard|last6=Kolter|first6=Roberto|date=June 2004|title=Genes involved in formation of structured multicellular communities by Bacillus subtilis|journal=Journal of Bacteriology|volume=186|issue=12|pages=3970–3979|doi=10.1128/JB.186.12.3970-3979.2004|issn=0021-9193|pmc=419949|pmid=15175311}}{{Cite journal|last1=Branda|first1=Steven S.|last2=Chu|first2=Frances|last3=Kearns|first3=Daniel B.|last4=Losick|first4=Richard|last5=Kolter|first5=Roberto|date=February 2006|title=A major protein component of the Bacillus subtilis biofilm matrix|journal=Molecular Microbiology|volume=59|issue=4|pages=1229–1238|doi=10.1111/j.1365-2958.2005.05020.x|issn=0950-382X|pmid=16430696|s2cid=3041295|doi-access=free}}{{Cite journal|last1=Romero|first1=Diego|last2=Aguilar|first2=Claudio|last3=Losick|first3=Richard|last4=Kolter|first4=Roberto|date=2010-02-02|title=Amyloid fibers provide structural integrity to Bacillus subtilis biofilms|journal=Proceedings of the National Academy of Sciences|volume=107|issue=5|pages=2230–2234|doi=10.1073/pnas.0910560107|issn=0027-8424|pmc=2836674|pmid=20080671|bibcode=2010PNAS..107.2230R|doi-access=free}}[http://esciencenews.com/articles/2008/12/22/small.molecule.triggers.bacterial.community Science News, Dec. 22, 2008] 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.{{Cite journal|last1=Hall-Stoodley|first1=Luanne|last2=Costerton|first2=J. William|last3=Stoodley|first3=Paul|date=February 2004|title=Bacterial biofilms: from the natural environment to infectious diseases|journal=Nature Reviews. Microbiology|volume=2|issue=2|pages=95–108|doi=10.1038/nrmicro821|issn=1740-1526|pmid=15040259|s2cid=9107205}}{{Cite journal|last1=López|first1=Daniel|last2=Vlamakis|first2=Hera|last3=Kolter|first3=Roberto|date=2010|title=Biofilms|journal=Cold Spring Harbor Perspectives in Biology|volume=2|issue=7|page=a000398|doi=10.1101/cshperspect.a000398|issn=1943-0264|pmc=2890205|pmid=20519345}}

  • {{cite journal | last1 = O'Toole | first1 = GA | last2 = Kolter | first2 = R | year = 1998 | title = Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signaling pathways: a genetic analysis | journal = Mol Microbiol | volume = 28 | issue = 3| pages = 449–61 | pmid = 9632250 | doi = 10.1046/j.1365-2958.1998.00797.x | s2cid = 43897816 }}
  • {{cite journal | last1 = O'Toole | first1 = GA | last2 = Flagellar | first2 = Kolter R. | year = 1998 | title = Pseudomonas aeruginosa biofilm development | journal = Mol Microbiol | volume = 30 | issue = 2| pages = 295–304 | pmid = 9791175 | doi = 10.1046/j.1365-2958.1998.01062.x | s2cid = 25140899 }}
  • {{cite journal | last1 = O'Toole | first1 = G | last2 = Kaplan | first2 = HB | last3 = Kolter | first3 = R | year = 2000 | title = Biofilm formation as microbial development | journal = Annu Rev Microbiol | volume = 54 | pages = 49–79 | pmid = 11018124 | doi = 10.1146/annurev.micro.54.1.49 }}
  • {{cite journal | last1 = Branda | first1 = SS | last2 = González-Pastor | first2 = JE | last3 = Ben-Yehuda | first3 = S | last4 = Losick | first4 = R | last5 = Kolter | first5 = R | year = 2001 | title = Fruiting body formation by Bacillus subtilis | journal = Proc Natl Acad Sci USA | volume = 98 | issue = 20| pages = 11621–6 | pmid = 11572999 | doi = 10.1073/pnas.191384198 | pmc = 58779 | bibcode = 2001PNAS...9811621B | doi-access = free }}

== 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. Some cell types were found localized in clusters in different physical locations and time points during biofilm development. 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.

  • {{cite journal | last1 = Vlamakis | first1 = H | last2 = Aguilar | first2 = C | last3 = Losick | first3 = R | last4 = Kolter | first4 = R | year = 2008 | title = Control of cell fate by the formation of an architecturally complex bacterial community | journal = Genes Dev | volume = 22 | issue = 7| pages = 945–53 | pmid = 18381896 | doi = 10.1101/gad.1645008 | pmc = 2279205 }}
  • {{cite journal | last1 = López | first1 = D | last2 = Vlamakis | first2 = H | last3 = Losick | first3 = R | last4 = Kolter | first4 = R | year = 2009 | title = Paracrine signaling in a bacterium | journal = Genes Dev | volume = 23 | issue = 14| pages = 1631–1638 | pmc = 2714712 | pmid = 19605685 | doi = 10.1101/gad.1813709 }}
  • {{cite journal | last1 = López | first1 = D | last2 = Vlamakis | first2 = H | last3 = Losick | first3 = R | last4 = Kolter | first4 = R | year = 2009 | title = Cannibalism Enhances Biofilm Development in Bacillus subtilis. | journal = Mol Microbiol | volume = 74 | issue = 3| pages = 609–618 | pmc = 2983100 | pmid = 19775247 | doi = 10.1111/j.1365-2958.2009.06882.x }}
  • {{cite journal | last1 = van Gestel | first1 = J | last2 = Vlamakis | first2 = H | last3 = Kolter | last4 = Collectives | first4 = Cell | year = 2015 | title = Bacillus subtilis Uses Division of Labor to Migrate | journal = PLOS Biol | volume = 13 | issue = 4 | page = 4 | doi = 10.1371/journal.pbio.1002141 | pmid = 25894589 | pmc = 4403855 | doi-access = free }}
  • {{cite journal | last1 = Lyons | first1 = NA | last2 = Kraigher | first2 = B | last3 = Stefanic | first3 = P | last4 = Mandic-Mulec | first4 = I | last5 = Kolter | year = 2016 | title = Bacillus subtilis | journal = Curr Biol | volume = 26 | issue = 6| pages = 733–42 | pmid = 26923784 | doi = 10.1016/j.cub.2016.01.032 | pmc = 4803606 }}

== 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.

  • {{cite journal | last1 = Hogan | first1 = DA | last2 = Kolter | first2 = R | year = 2002 | title = Pseudomonas-Candida interactions: an ecological role for virulence factors | journal = Science | volume = 296 | issue = 5576| pages = 2229–32 | pmid = 12077418 | doi = 10.1126/science.1070784 | bibcode = 2002Sci...296.2229H | s2cid = 23124129 }}
  • {{cite journal | last1 = Shank | first1 = EA | last2 = Klepac-Ceraj | first2 = V | last3 = Collado-Torres | first3 = L | last4 = Powers | first4 = GE | last5 = Losick | first5 = R | last6 = Kolter | year = 2011 | title = Bacillus subtilis forming biofilms are mediated mainly by members of its own genus | journal = Proc Natl Acad Sci U S A | volume = 108 | issue = 48| pages = E1236–43 | pmid = 22074846 | doi = 10.1073/pnas.1103630108 | pmc = 3228442 | doi-access = free }}
  • {{cite journal | last1 = Traxler | first1 = MF | last2 = Watrous | first2 = JD | last3 = Alexandrov | first3 = T | last4 = Dorrestein | first4 = PC | last5 = Kolter | first5 = R | year = 2013 | title = Interspecies interactions stimulate diversification of the Streptomyces coelicolor secreted metabolome | journal = mBio | volume = 4 | issue = 4| page = 4 | doi = 10.1128/mbio.00459-13 | pmid = 23963177 | pmc = 3747584 }}
  • [https://elifesciences.org/articles/17473 Segev E, Wyche TP, Kim KH, Petersen J, Ellebrandt C, Vlamakis H, Barteneva N, Paulson JN, Chai L, Clardy J, Kolter R. Dynamic metabolic exchange governs a marine algal-bacterial interaction. 2017. eLife.]
  • [http://mbio.asm.org/content/8/4/e00723-17.short Lyons NA, Kolter R. Bacillus subtilis Protects Public Goods by Extending Kin Discrimination to Closely Related Species. mBio. 2017; 8 no. 4e00723-17.]

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. 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.{{Cite web|url=http://www.msi.harvard.edu/downloads/Wine%20Seminar2016.pdf|title=Appreciating Wine and the Microbes that Make it. Harvard Microbial Sciences Initiative.}} 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.{{Cite web|url=https://www.statnews.com/2017/12/21/microbes-human-life/|title=Microbes gave us life|last1=Chimileski|first1=Scott|last2=Koter|first2=Roberto|date=2017-12-21|website=STAT|access-date=2019-07-31}}

= Books =

  • [https://www.amazon.com/Germ-Stories-Arthur-Kornberg/dp/1891389513/ref=sr_1_1?s=books&ie=UTF8&qid=1500678165&sr=1-1&keywords=germ+stories Germ Stories] by Arthur Kornberg, 2007 (provided photography) {{ISBN|1891389513}}
  • [http://www.hup.harvard.edu/catalog.php?isbn=9780674064096 March of the Microbes] by John Ingraham (authored a foreword) {{ISBN|0674064097}}
  • [http://www.asmscience.org/content/book/10.1128/9781555818470 Microbes and Evolution:The World Darwin Never Saw], 2012, co-edited with Stanley Maloy, American Society of Microbiology Press, {{ISBN|1891389513}}
  • [http://www.hup.harvard.edu/catalog.php?isbn=9780674975910 Life at the Edge of Sight: A Photographic Exploration of the Microbial World], 2017, coauthored with Scott Chimileski, Harvard University Press, {{ISBN|067497591X}}

= Museum exhibitions =

From 2014 through 2018, Kolter and Scott Chimileski spearheaded two public exhibitions at the Harvard Museum of Natural History. [https://hmnh.harvard.edu/world-drop-photographic-explorations-microbial-life 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.{{Cite web|url=https://news.harvard.edu/gazette/story/2017/10/harvard-scientists-turn-beauty-of-microbes-into-museum-material/|title=Harvard scientists turn beauty of microbes into museum material|date=2017-10-27|website=Harvard Gazette|access-date=2019-07-31}} Subsequently, [https://hmnh.harvard.edu/news/microbial-life-universe-edge-sight 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. These exhibitions have traveled internationally at the Eden Project in the UK and EAFIT University in Medellín, Colombia, among other locations.{{Cite web|url=https://cornishstuff.com/weekendstuff/2018/11/03/world-in-a-drop-stunning-microbial-photo-exhibition/|title=World in a Drop – Stunning Microbial Photo Exhibition {{!}}|last=miloperrin|date=2018-11-03|website=Weekend Stuff|access-date=2019-07-30}}{{Cite web|url=http://www.eafit.edu.co:80/noticias/agenciadenoticias/2018/zoom-fotografico-al-mundo-microbiano|title=Zoom fotográfico al mundo microbiano|last=EAFIT|first=Universidad|website=www.eafit.edu.co|language=es-ES|access-date=2019-07-31}}{{Cite web|url=https://www.edenproject.com/media/2018/11/drop-into-eden-for-stunning-new-microbial-photo-exhibition|title=Drop into Eden for stunning new microbial photo exhibition|date=2018-11-02|website=Eden Project|access-date=2019-07-31}}

Chimileski and Kolter were also advisors and contributed imagery for Invisible Worlds at the Eden Project, a permanent exhibition sponsored by the Welcome Trust.{{Cite web|url=https://www.edenproject.com/visit/whats-here/invisible-worlds-exhibition/a-closer-look|title=Invisible Worlds: zooming in for a closer look|date=2018-11-05|website=Eden Project|access-date=2019-07-31}} Their still and time-lapse imagery was featured in the [http://www.oum.ox.ac.uk/bacterialworld/ Bacterial World Exhibition] at the Oxford University Museum of Natural History in 2018, and in the [https://www.cdc.gov/museum/exhibits/world-unseen.htm 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 [https://harvardx.harvard.edu/ HarvardX] on fermentation and microbial foods.{{Cite web|url=https://news.harvard.edu/gazette/story/2017/11/humans-need-microbes-for-survival-and-a-decent-dinner/|title=Humans need microbes for survival — and a decent dinner|date=2017-11-08|website=Harvard Gazette|access-date=2019-07-31}} He is a regular instructor at the Microbial Diversity Course at the Marine Biological Laboratory in Woods Hole, Massachusetts, the EMBO-FEBES [http://events.embo.org/16-microbiol/ summer microbiology course] in Spetses, Greece and the John Innes/Rudjer Bošković Summer School in Applied Molecular Microbiology in Dubrovnik, Croatia. In 2000, he received the ASM International Professorship Award.

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.{{Cite web|url=https://jb.asm.org/content/board-editors|title=Journal of Bacteriology, Editorial Board|website=jb.asm.org|access-date=2017-07-22}}

Sources

{{Reflist|30em}}