Of Slot Machines and Broken Test Tubes

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1 Of Slot Machines and Broken Test Tubes The Life and Times of Salvador Luria S Mahadevan The year 2012 was the birth centenary of the pioneer microbiologist/molecular geneticist, Salvador Luria whose life exemplified the axiom that both brilliance and serendipity have a role in defining success. In 1943 Luria along with physicist Max Delbrück demonstrated that bacteria are ideal model organisms to address fundamental questions involving heredity, triggering the emergence of the new field of molecular genetics. Their famous Fluctuation Test carried out with the bacterium Escherichia coli provided statistical evidence for the spontaneous nature of mutations, supporting the Darwinian idea of natural selection. His observations on the role of host modification in determining bacteriophage host specificity and its epigenetic transmission ultimately led to the discovery of bacterial restriction-modification systems that opened the door to recombinant DNA technology. This article is an attempt to capture the myriad contributions to science and science education by one of the founding fathers of modern genetics. The field of genetics formally started at the turn of the 20th century with the rediscovery of Mendel s laws of heredity in Mendel s laws provided for the first time in biology a theoretical framework to quantitatively analyze the nature and transmission of genetic information. The first half of the 20th century was dominated by genetic studies on plants, flies and fungi; microorganisms were conspicuous by their absence in these studies. The term microbial genetics was considered an oxymoron as bacteria did not show any signs of possessing chromosomes. This was compounded by the fact that they are microscopic and hence any phenotype they exhibit is the collective property of millions of bacterial cells in a colony or culture. S Mahadevan is a professor of genetics, Indian Institute of Science. His research interests are microbial genetics, physiology and evolution. He is also passionate about history of science and science education. Keywords Bacterial genetics, fluctuation test, spontaneous mutation, bacteriophage restriction. 395

2 The most significant contribution of Luria was the demonstration in 1943 of mutations in bacteria conferring resistance to virus. 1 See Resonance, Vol.12, No.9, Bacteria also often exhibit transient adaptive behaviour in response to an environmental challenge, reminiscent of the inheritance of acquired characters outlined by the renowned French zoologist Lamarck in Any evidence for genetic transmission of traits by bacteria had to overcome the adaptive bias. This was in spite of the work of Massini who in 1907 showed the genetic nature of the loss of lactose catabolism in mutants of Escherichia coli and the genetic transmission of the rough colony phenotype in cultures of Streptococcus pneumoniae by Griffith in 1928 that ultimately led to the identification of the chemical nature of the genetic material by Avery et al 1 in The most significant contribution of Luria was the demonstration in 1943 of mutations in bacteria conferring resistance to virus. This classic work in collaboration with Delbrück launched the use of bacteria in several experiments targeted at understanding fundamental aspects of living organisms, laying the foundations of molecular genetics. In the words of Gunther Stent, Luria and Delbrück did for bacterial genetics what Mendel had done for genetics namely to show for the first time what kind of experimental arrangements, what kind of data treatment, and above all, what kind of sophistication are required for obtaining meaningful and unambiguous results [1]. Early Life Salvador Luria was born in a middle class Jewish family in Turin, Italy, on August 13, His parents David and Esther were keen that he received a good education. Though his performance in natural sciences was average, school education did give him a strong liking for arts and literature that lasted all through his life. His school years were turbulent times with the growth of the fascist movement in Italy. Young Salvatore (as he was known at that time) was greatly influenced by the liberal ideology of many of his teachers who fought against fascism. This influence also had a life-long impact on Luria as he championed the cause of justice and equality for all, even during the later stages of his career. 396 RESONANCE May 2014

3 Though Luria did not exhibit any extraordinary capabilities as a student, he enrolled for medical education as desired by his parents and obtained his medical degree from Turin, graduating with honours in As he was not keen to be a clinician and was more interested in basic sciences, under the influence of his physicist friend Ugo Fano, Luria moved to Rome to study physics and mathematics with the eventual goal of specializing in radiation medicine. In Rome, he could spend some time in the laboratory of the legendary Enrico Fermi. Soon, Luria realized that his ability to deal with physics was weak, especially because mathematics was not his natural language. About this Luria writes, Yet that year among physicists proved to be the critical turning point in my life. It taught me to think a bit in the way physicists do, a way more analytical than the way of biologists [2]. Luria focused his attention on radiation physics and was drawn to the study of the effect of radiation on living organisms. In the course of these studies, he was exposed to the work of the American geneticist Herman Muller who could demonstrate the mutagenic action of X-rays and the path-breaking work of the German physicist Max Delbrück 2 who was using radiation to discern the physical parameters of the gene. Based on his results, Delbrück had proposed that mutations are the results of quantum transitions in the gene induced by radiation. This exposure opened Luria s way to the Holy Grail of biophysics. At this point he knew exactly what he wanted to do; I swore that I would be a knight of the Grail. 2 See Resonance, Vo.4, No.11, Luria s exposure to the work of Delbrück coincided with his introduction to bacterial viruses or bacteriophages (that infect and kill the bacterial host) through a chance meeting with his friend Geo Rita, a bacteriologist. Luria spent the following week in Geo Rita s lab working on phages and mastered the methods to grow and count phages it was love at first sight. Both Luria and Delbrück independently came up with the idea that the phage will be a good experimental system to study the role of radiation on genes as the phage represented a rudimentary form of a living system. Armed with a fellowship from the Italian government, in 397

4 1938, Luria was ready to set sail to the United States to work with Delbrück who had recently immigrated to USA from Germany. Unfortunately, Luria had to delay his plans due to the political turmoil in Italy. In 1938, the fascist government of Italy entered into an alliance with Nazi Germany and promulgated the Racial Manifesto, denying all rights to Jewish citizens of Italy. Luria traveled to Paris and with a fellowship from the French government, could work at the Institute of Radium on the effects of radiation on phage C16. In 1940, France was overrun by Germany and Luria managed to escape on a bicycle to Marseilles, where, after some bureaucratic delays, he obtained a visa to travel to the USA. Leaving France, Luria traveled to Spain and Portugal and could board the Greek ship Nea Hella sailing to New York from Lisbon. The ship docked at the New York harbour on the morning of September 12, While registering for citizenship, Luria was offered a change of name; he became Salvador Edward Luria. The primary goal of Luria and Delbrück was to understand the steps involved in the growth and replication of the phage inside the host cell. Supported by a recommendation letter from Fermi, Luria could start work at the College of Physicians and Surgeons of Columbia University, with a fellowship from the Rockefeller Foundation. He could finally meet Max Delbrück in December 1940 during the American Physical Society annual meeting in Philadelphia. Delbrück was teaching physics at Vanderbilt University, Nashville, Tennessee. The duo planned to meet the following summer at the Biological Laboratory of Cold Spring Harbor, Long Island, which was fast becoming the Mecca of the emerging discipline of molecular biology. This was the beginning of a long collaboration; their work continued in Vanderbilt at times and in Bloomington, Indiana, where Luria took up an entry level faculty position. The Origin of Bacterial Mutants The primary goal of Luria and Delbrück was to understand the steps involved in the growth and replication of the phage inside the host cell. How can one phage infecting a sensitive bacterial 398 RESONANCE May 2014

5 cell end up producing one hundred progeny phages? One way of tracking the infection by the phage is to use two strains of phages to infect the bacterium and follow the subsequent events. In the course of these studies, one of the critical observations made was that, upon spreading bacteria sensitive to a specific phage on a plate saturated with the phage, one could observe a few colonies of survivor bacteria. They appeared to have inherited the property of resistance to the specific phage, as all progeny bacteria derived from the phage-resistant colony appeared to breed true even when grown in the absence of phage. Does it mean that there is a gene for sensitivity to phage and mutations in the gene can lead to resistance to a specific phage and not others? What will be the nature of these mutations? Are they spontaneous and therefore pre-exist in the bacterial population or do they arise only after exposure to the phage? If they are spontaneous and pre-exist in the culture, it will be supportive of the Darwinian idea of natural selection. If they are indeed a response to the presence of the phage, it will suggest a Lamarckian adaptive mechanism. An experimental demonstration of the prevailing mechanism will go a long way in establishing the role of bacteria as a model system to study one of the most fundamental issues in biology. The experimental system that Luria chose was the bacterium Escherichia coli, a commensal present in the mammalian intestine and the deadly phage T1 that can run through a sensitive E. coli culture like wildfire. The question was, how can one differentiate between the two mutually exclusive mechanisms? The scheme that Luria came up with is as follows. If the resistance to phage is induced upon exposure to the phage, every cell has a finite but small probability of developing resistance upon exposure. In such a case, the number of phage-resistant mutants in different replicates will depend entirely on the number of cells plated and will follow a Poisson distribution around the mean. On the contrary, if the phage-resistant mutants arise spontaneously, they could appear at any point of growth before exposure to the phage and therefore their number will depend, in addition to the number of cells plated, on the number of generations grown. This The experimental system that Luria chose was the bacterium Escherichia coli, a commensal present in the mammalian intestine and the deadly phage T1. 399

6 3 A gambling device seen in many casinos where the player deposits a coin and cranks the handle. Most times nothing happens. If the player is lucky, the machinewillreturnalargersum than what was deposited an outcome known as jackpot. Figure 1. Experimental strategy to differentiate between mutations that are induced by selection (A) and mutations (B) that occur spontaneously before selection (adapted from [1]). is because the mutants appearing at earlier time points will grow and will be amplified by the time of plating. Luria s strategy was to have several independent cultures inoculated with small numbers of sensitive bacteria and count the number of phage-resistant mutants by plating the cultures, grown for different periods of time, on Petri dishes seeded with the phage. If indeed the number of resistant mutants does depend on the number of generations grown, it will be indicative of the mutations being spontaneous. However, to the annoyance of Luria, the number of resistant colonies fluctuated widely in different replicates, making any meaningful conclusion impossible. Serendipity played a part in the resolution of the issue. It so happened that Luria attended a ball for faculty at Bloomington and one of the attractions at the function was a slot machine. While observing one of his colleagues having a go at the slot machine 3, Luria was struck by the fact that the returns from the slot machine were similar to the distribution of mutants that he had observed. Most of the time the slot machine did not yield anything or there were low returns. Very rarely did the player hit a jackpot. This output resembled the fluctuating numbers of mutants he saw. The solution became obvious. Most of the time, no mutations happened as the frequency involved was small. The rare large numbers of mutants observed were similar to a jackpot and represented rare mutants that arose rather early and were clonally amplified (see Figure 1). Eventually it was realized that these fluctuations were not due to any uncontrolled conditions of our experiments, but on the contrary, large fluctuations are a consequence of the mutation hypothesis and that a quantitative study of the fluctuations may serve to test the hypothesis [2]. Luria was overjoyed and communicated his observations to Delbrück. The reply from Delbrück came with a theoretical analysis of the problem. Though Delbrück did not derive the distribution function for the jackpot outcome observed, he could calculate the 400 RESONANCE May 2014

7 mutation frequency from his analysis. Their joint paper was published in 1943 with the interesting footnote Theory by M.D., Experiments by S.E.L.[3]. Luria and Delbrück shared the 1969 Nobel Prize with Alfred Hershey, another phage crusader, for their contributions to molecular genetics. Though the solution to the problem was triggered by a serendipitous event, it was Luria s brilliance that enabled him to extract the design of the experiment. The Phage Group To appreciate the full significance of Luria s work, one should look at it from the point of our understanding of genetics that prevailed during the early nineteen forties. Though classical genetics had advanced significantly, the chemical nature of the gene and the way it functions were unknown. One major breakthrough was the observation made in 1908 by Archibald Garrod that inherited disorders such as phenylketoneurea (which he termed as inborn errors in metabolism) could be correlated with deficient enzymes, implying a direct relation between the Mendelian factors and enzymes. This forgotten observation of Garrod was reinforced almost four decades later by the elegant work of George Beadle and Edward Tatum, carried out using the bread mold Neurospora, resulting in the famous one-gene-one-enzyme hypothesis [1]. Considered as the last strongholds of Lamarckism, bacteria were not in the picture as a system amenable for genetic analysis, partly reinforced by the strong opinion of the British physical chemist Sir Cyril Hinshelwood who believed that bacteria have no genes and their phenotypes can be correlated to biochemical reaction kinetics. It was heresy to contradict such strongly held beliefs. In his famous work Evolution: The Modern Synthesis published in 1943, the celebrated evolutionary biologist Julian Huxley remarks that the process of variation, heredity and evolution in bacteria are quite different from the corresponding processes in multicellular organisms. The Luria Delbrück experiment categorically established the role of microorganisms in genetic analysis and launched the new field of molecular genetics. The following decade witnessed The Luria Delbrück experiment categorically established the role of microorganisms in genetic analysis and launched the new field of molecular genetics. 401

8 several path-breaking results, culminating in the discovery of the double helical structure of DNA ten years later by James Watson (the first graduate student of Luria) and Francis Crick in Encouraged by the success, Delbrück, along with Luria and Alfred Hershey, championed the use of phage in molecular biology and initiated the phage group which was joined by many devotees. Several phenomena such as recombination and repair in bacteria and phage came to light as a result of the onslaught. Hershey along with Martha Chase could elegantly demonstrate that it is the nucleic acid that enters the host cell during phage infection and the protein coat is left behind. The Cold Spring Harbor Laboratories became the central hub and hosted annual meetings on the Genetics of Bacteria and Phages as well as phage courses and workshops. Restriction of Phage by the Host The observation of Luria and his student Mary Human led to the identification of the first hostencoded restriction system, which is known today as mcr. In 1950, Luria accepted the offer of a faculty position as professor of bacteriology from the University of Illinois, Urbana, and continued his research on host phage interactions. In the course of analyzing the fate of host DNA during phage T2 and T6 infection, Luria came up with another interesting observation. In one class of bacterial mutants, upon infection by the phage, the cells lysed, but did not yield any progeny phage. The host used in these experiments was the standard strain of E. coli B. One day, the tube in which the host strain was grown broke and Luria was forced to use a strain of Shigella disenteriae that was available. To his enormous surprise, the Shigella strain allowed lysis by the phage grown on the E. coli B mutant that could not form plaques on either the mutant or wild-type strain of E. coli B. In some cases, the age of the host also influenced the ability of the phage progeny to form plaques. Thus, it was apparent that the host was marking the phage progeny in some non-genetic manner that could be transmitted to the next generation. Today such nongenetic marking of DNA and its transmission is known as epigenetics and has become a fad, with some molecular biologists even claiming it as a 21st century phenomenon! The 402 RESONANCE May 2014

9 observation that Luria and his student Mary Human described in their 1952 paper in the Journal of Bacteriology led to the identification of the first host-encoded restriction system, which is known today as mcr, that targets DNA-carrying cytosine residues that are hydroxymethylated, as happens in the case of T2 and T6 genomes. Glycosylation of the hydroxymethylated cytosine residues can prevent the cleavage and loss of host function involved in glycosylation can lead to susceptibility, as it happened in the case of the mutants that Luria and Human were studying. Subsequently, the restriction-modification system known as Type I system was discovered by Werner Arber and colleagues using the lambda phage. The isolation by Hamilton Smith and colleagues of the first Type II restriction enzyme RI and the demonstration of its use in mapping the SV 40 viral genome by Daniel Nathans and colleagues heralded the advent of the recombinant DNA technology. For a molecular biologist today, it is difficult to imagine life without these enzymes as they have become very much tools of the trade. Arber, Smith, and Nathans shared the 1978 Nobel Prize in Physiology or Medicine for their discoveries, which were in a sense, triggered by the work of Luria. This is an example where meticulous analysis of what may originally be considered as a rather esoteric observation, can have a revolutionary impact and open new avenues of research. Work on Bacterial Membranes and Colicins In 1958, the biology department of Massachusetts Institute of Technology (MIT) invited Luria to start a new programme in microbiology and subsequently offered him the position as Programme Chair. The extraordinary success that Luria had in terms of setting up the labs and hiring talented young faculty colleagues demonstrated his outstanding capability as an institution builder. At MIT, Luria decided to move away from phage work and focus on bacterial membranes. He found the issue of integral membrane proteins challenging from a structural and functional angle. Luria chose to study colicins that are water-soluble anti- Meticulous analysis of what may originally be considered as a rather esoteric observation, can have a revolutionary impact and open new avenues of research. 403

10 4 See Resonance, Vol.8, No.7, microbial peptides encoded by genetic elements known as episomes or plasmids present in enteric bacteria. Colicins worked on the membranes of susceptible bacteria by jamming them, preventing uptake of many essential substrates. He started the work in 1963 while on sabbatical at the Pasteur Institute in Paris, hosted by Jacques Monod 4. Back at MIT, Luria and his younger colleagues could establish that colicins formed channels across membranes causing the leakage of ions, thereby disrupting membrane potential that is essential for sustaining several key functions of the cell. Cancer Research Center at MIT In 1972, upon receiving a request from MIT, Luria established one of the finest laboratories for cancer research by remodeling a chocolate factory close to MIT in Cambridge, Massachusetts. In addition to his MIT colleague Phillips Robbins, he could recruit virologist David Baltimore and immunologist Herman Eisen to the Cancer Center. Robert Weinberg and Phillip Sharp joined the team subsequently. Cancer research at the centre flourished and several discoveries reverse transcriptase, oncogenes and RNA splicing followed in quick succession and so did several Nobel Prizes. Luria remained as its director till he retired in Though he did not take part in cancer research directly, the success of the center was to a large extent due to his outstanding leadership. Author, Teacher, and Mentor In addition to his brilliant scientific contributions, Luria is also remembered as a gifted teacher and a wonderful mentor. In addition to his brilliant scientific contributions, Luria is also remembered as a gifted teacher and a wonderful mentor. His undergraduate biology course was very popular and his lecture series was published in 1975 titled 36 Lectures in Biology on the same lines as the famous Feynman Lectures in Physics. His book Life the Unfinished Experiment written for the non-specialist reader and the autobiographical A Slot Machine, A Broken Test Tube (reviewed in this issue) give a firsthand account of his science and philosophy. One of his famous statements is, A 404 RESONANCE May 2014

11 lesson I learnt was that in research, one must leave people alone, especially good people. The better the student, the more important it is to leave them to themselves [2]. Epilogue Luria s world went beyond science; he was a great admirer of art and literature and believed that science and humanities are two facets of life that should always go together. He was a political activist who was not afraid to raise his voice against prejudice and injustice though at times there was a cost he had to pay for his principled stand. The world lost a pioneer scientist, teacher, mentor and crusader when Salvador Luria succumbed to heart failure on Feb. 6, He passed away at his Lexington, Massachusetts home and was survived by his psychologist wife Dr. Zella Hurwitz whom he married in 1945 and their only son Daniel who is an economist. Suggested Reading [1] G Stent and R Calendar, Molecular Genetics An Introductory Narrative, W H Freeman and Company, San Francisco, [2] S E Luria, A Slot Machine, A Broken Test Tube, Harper Collins, [3] S Luria and M Delbrück, Mutations of bacteria from virus sensitivity to virus resistance. Genetics, Vol.28, pp , [4] The Salvador Luria papers Address for Correspondence S Mahadevan MRDG Indian Institute of Science Bangalore , India 405

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