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International Prize for biology

Past Recipients

Recipient

The Committee on the International Prize for Biologyof Japan Society for the
Promotion of Science awards
the 2010 International Prize for Biology in the field of "Biology of Symbiosis"
to
Dr. Nancy Ann MORAN
William H. Fleming Professor, Department of Ecology and Evolutionary Biology,
Yale University, U.S.A.

  On Thursday, October 7, 2010, at a meeting of the Committee on the International Prize for Biology (chaired by Dr. Takashi Sugimura, Secretary General, The Japan Academy) of Japan Society for the Promotion of Science decided to present the 26th (2010) International Prize for Biology to Dr. Nancy Ann Moran, American citizen, William H. Fleming Professor, Department of Ecology and Evolutionary Biology, Yale University, USA. The field of specialization for the 26th Prize is "Biology of Symbiosis."

rof. Nam-Hai Chua
 

 
 

Process of Selection

  The Selection Committee, established by the Committee on the International Prize for Biology and chaired by Makoto Asashima, Director of Research Center for Stem Cell Engineering, AIST, distributed a total of 1,957 recommendation forms to Japanese and foreign universities, research centers, academic associations, individual researchers, and international academic organizations involved in the subject field of biology, and received a total of 55 recommendations in response. As some of these recommendations named the same individuals, the actual number of individuals recommended was 46, from 16 countries. The Selection Committee met a total of four times and very carefully reviewed all the candidates. Ultimately, the Committee decided to recommend Dr. Nancy Ann Moran as the recipient of the 26th International Prize for Biology.

 

Achievements Recognized by the Award

  Dr. Moran has contributed greatly to the advancement of the biology of symbiosis in recent years through her studies of intimate coevolutionary relationships between insects and the endosymbiotic bacteria that live within them, studies which have yielded by far the largest number of outstanding research results in this field thanks to Dr. Moran’s versatile approach, which draws on molecular biology, genomics, and experimental and theoretical biology.


  The most noteworthy of her wide-ranging achievements include demonstrating the ancient evolutionary origins, dating back several hundred million years, of obligate bacterial symbionts in aphids and other insects, and elucidating the coevolutionary process involved; providing an understanding of metabolic complementarity in symbiosis and the molecular basis of this interdependence; sequencing whole genomes and determining biological functions in various bacterial symbionts; and revealing the effects of bacterial symbionts on ecology and adaptation of their hosts. In particular, Dr. Moran has succeeded in using a population genetics approach to explain theoretically the special patterns of genome evolution, such as rapid molecular evolution, reduced genome size, and biased nucleotide composition, that are seen in various bacterial symbiont lineages. This breakthrough has provided an integrated understanding of the reductive genome evolution seen in many microbial groups besides bacterial symbionts of insects, including endoparasitic bacteria like Rickettsia, and even extending to organelles such as mitochondria and chloroplasts.


  Thus, Dr. Moran’s research has shown symbiosis to be an important source of evolutionary novelty, has provided concrete evidence of its contributions to ecological niche expansion, and has established principles common to the diverse spectrum of symbiotic relationships. These achievements have contributed enormously to the advancement of many fields, including evolutionary biology, ecology, microbiology, and genomics.

 

Ceremony and Commemorative Symposium

  The award ceremony will be held on Monday, December 6, 2010, at the Japan Academy (7-32 Ueno Koen, Taito-ku, Tokyo). Each year, Their Majesties the Emperor and Empress attend the ceremony and a party in honor of the award recipient.
  To commemorate the award to Dr. Nancy Ann Moran, the 26th International Prize for Biology Commemorative Symposium on Biology of Symbiosis will take place on Tuesday, December 7 and Wednesday, December 8, 2010, at Tsukuba International Congress Center.

 

DATE OF BIRTH :  December 21, 1954
NATIONALITY :  United States of America
PRESENT POSITION :  William H. Fleming Professor,
Department of Ecology and Evolutionary Biology,
Yale University, USA
 

HONORS AND AWARDS

1988   American Society of Naturalists President's Award
1997 – 2002 John D. and Catherine T. MacArthur Fellow
2001 University of Arizona Regents’ Professor
2004 Member of the American Academy of Microbiology
2004 Member of the National Academy of Science
2006 Galileo Circle Faculty Fellow, College of Science, University of Arizona
2006 Member of the American Academy of Arts and Sciences
2007 Fellow of the American Association for the Advancement of Science
2008 University of Arizona Alumni Association Extraordinary Faculty Award

 

Research Acheivements

  Dr. Moran’s primary research interest is the biology of the intimate coevolution that occurs between animals, especially insects, and the bacterial symbionts that live within their bodies. Using an array of approaches including molecular biology, genomics, and experimental and theoretical biology, she has achieved outstanding results concerning the evolutionary origins of symbiosis, its universality in the animal kingdom, and its impact on the evolution and ecology of both hosts and symbionts, among other topics. Together with shedding new light on the consequences of coevolution, based on these discoveries she has made major and far-reaching contributions to the advancement of the biology of symbiosis, including the development of a general theory of microbial genome evolution.


1) The Ancient Evolutionary Origins of Symbiosis
  Using molecular phylogenetic techniques and the fossil record of tiny insects preserved in amber, Dr. Moran established that the coevolution of aphids and the bacterial endosymbiont Buchnera,which is necessary to their survival, has a very ancient history (over 100 million years), and showed this to be a case of stable long-term cospeciation (Moran et al. 1993). This discovery led to a series of reports of similar cospeciation in various host-symbiont pairs besides aphids and Buchnera. For example, Dr. Moran has demonstrated ancient evolutionary origins, dating back at least 270 million years, for the bacterial endosymbionts common to the large group of insects known as the Homoptera, which includes cicadas, spittlebugs, leafhoppers, and planthoppers, and she has suggested that this symbiosis was probably already established during the evolution of the earliest land plants and plant-feeding insects (Moran et al. 2005). Once the symbiosis became established, the host insect is thought to have inherited the bacterial symbionts by vertical transmission over millions or hundreds of millions of generations. Such a pattern, which recurs in various groups of insects and other invertebrates, points to the strong possibility that the acquisition of bacterial symbionts may have been important to adaptive radiation and diversification in these organisms.


2) Metabolic Complementarity in Symbiosis
  Dr. Moran’s group has found striking complementarity in the metabolic capabilities of bacterial symbionts and host insects, and also in those of different bacterial symbionts resident in the same host. They have shown by genome analysis that coresident bacterial symbionts, even if they are of unrelated species, may possess a complementary set of biosynthetic pathway gene clusters, or gene clusters complementarily involved in different steps of the same pathway. For example, in the glassy-winged sharpshooter and the cicada, one symbiont supplies the host with eight of the ten essential amino acids the host needs to survive and a second symbiont provides the remaining two, with both symbionts having the required metabolic pathways (Wu et al. 2006; McCutcheon and Moran 2007; McCutcheon et al. 2009). These findings can be seen as concrete evidence that the evolution of sophisticated symbiotic relationships becomes irreversible due to codependency among the partners.


3) Proposal of the Genome Reduction Theory for Bacterial Symbionts
  Starting in 1990s, the DNA sequences of obligate bacterial symbionts of various insects were found to share some unusual structural and evolutionary traits: in particular, they show rapid molecular evolution, with fast rates of change of DNA and protein sequences; they have a reduced genome size, having lost many of the genes present in free-living relatives; and the genomic DNA shows a biased nucleotide composition, favoring adenine-thymine over guanine-cytosine. Over the ensuing years, biologists had merely speculated as to whether these traits were related to the special lifestyle and environment of organisms that live inside a host’s cells, until Dr. Moran proposed that the genome evolution patterns of these endosymbionts could be explained in an integrated way by drawing on population genetics theory (Moran 1996). In population genetics, according to the effect known as “Muller’s ratchet,” in small asexual populations there is a high rate of fixation of mildly deleterious mutations, as these are not eliminated successfully; this effect has often been used as an argument for the value of sexual reproduction. Dr. Moran pointed out that, in general, in bacterial symbionts necessary to the host’s survival, the effective population size becomes tiny because the process of vertical transmission from the host mother to the egg acts as a strong bottleneck in each generation; further, that populations of symbionts in the same host become effectively clonal, or genetically identical, because they do not reproduce outside the host and there is no horizontal transfer between hosts, and therefore they can be seen as asexual, in that no useful genetic recombination can occur. She thus formulated the hypothesis that traits like rapid molecular evolution, reduced genome size, and biased nucleotide composition occur because the population genetic structure is constrained by the obligate symbiont lifestyle and Muller’s ratchet makes it difficult to remove a mildly deleterious mutation, correct a bias in mutation repair, or reacquire a lost gene (Mira et al. 2001). This hypothesis is now widely accepted, having been supported by subsequent genomic and other findings in many obligate symbiont and endoparasitic bacteria.


  Extremely rapid molecular evolution and reduced genome size are also seen in intracellular organelles such as mitochondria and chloroplasts, which are thought to be derived from symbiotic bacteria, and they can be explained there in the same way. The smallest known bacterial genomes belong to symbionts of psyllids, sharpshooters and cicadas; as they have fewer than 200,000 base pairs and 200 genes, the entities that possess them are almost organelles. Dr. Moran’s group was involved in determining all of these genomes (Nakabachi et al. 2006; McCutcheon and Moran 2007; McCutcheon et al. 2009). Dr. Moran has earned the highest regard for having proposed a general theory, supported by actual examples, that offers an integrated explanation of reductive genome evolution in symbiotic bacteria, the phenomenon observed in a wide range of bacterial genomes whereby free-living bacteria enter a symbiosis, become obligate symbionts, and are eventually reduced to entities not unlike organelles.


4) Environmental Adaptation of Hosts Benefited by Bacterial Symbionts
  In many species populations, a number of bacterial symbionts are normally present at different infection frequencies. Most are not essential to the host and are harbored by only some individuals in the population. For a long time, the impact and significance of this facultative symbiont infection remained unclear, but recent research by Dr. Moran’s own group and others has led to an appreciation of its variegated biological functions. In particular, Dr. Moran’s group is noted for having shown that the facultative bacterial symbiont Hamiltonella in aphids confers resistance to parasitic wasps on the aphid host (Oliver et al. 2003), and that this protection against the wasp larva relies on toxins encoded on a bacteriophage (Oliver et al. 2009). Dr. Moran and her coworkers have also found that the polymorphism of resistance to parasitic wasps and tolerance to high temperatures seen in natural populations of aphids can be explained in terms of the genetic polymorphism of facultative bacterial symbionts (Oliver et al 2005; Russell and Moran 2006); that these facultative bacterial symbionts can be transmitted horizontally within and between species (Moran and Dunbar 2006); and that their genomes show features similar to those of pathogenic and parasitic bacteria (Degnan et al. 2009, 2010). Dr. Moran has further demonstrated that obligate bacterial symbionts like Buchnera can give rise to striking ecological changes; for example, a new mutation in Buchnera in a host insect population dramatically affected the host’s tolerance of heat stress (Dunbar et al. 2007). The picture furnished by this series of studies shows that the symbiotic microbiotas present in many organisms in nature often have subtle but non-negligible effects on the ecological, macroscopic, and adaptive properties of the hosts.


  Thus, while supplying a wealth of concrete evidence from perspectives ranging from evolutionary ecology to genomics, Dr. Moran’s extensive high-level studies have shown that symbiosis, as an important source of evolutionary novelty, has promoted diversification in many groups of organisms and has also endowed them with the ability to exploit new ecological niches. Researchers in this field long tended to limit themselves to the enumerative description of phenomena, but by taking population genetic processes into account, Dr. Moran has succeeded in providing an integrated explanation of microbial symbiont lifestyles at the evolutionary ecology level and of evolutionary trends at the genome level, thus establishing common principles within diversity. The great influence that Dr. Moran has had, and no doubt will continue to have, on the biology of symbiosis makes her the leading player internationally in this field.

Representative Publications:

  1. Moran, N. and W. D. Hamilton. 1980. Low nutritive quality as defense against herbivores. Journal of Theoretical Biology 86: 247-254.
  2. Moran, N. A. 1988. The evolution of host alternation in aphids: evidence that specialization is a dead end. The American Naturalist 132: 681-706.
  3. Moran, N. A., M. A. Munson, P. Baumann and H. Ishikawa. 1993. A molecular clock in endosymbiotic bacteria is calibrated using the insect hosts. Proceedings of the Royal Society of London Series B: 253: 167-171.
  4. Moran, N. A. 1996. Accelerated evolution and Muller’s ratchet in endosymbiotic bacteria. Proceedings of the National Academy of Sciences USA 93: 2873-2878.
  5. Rispe, C. and N. A. Moran. 2000. Accumulation of deleterious mutations in endosymbionts: Muller’s ratchet with two levels of selection. The American Naturalist 156: 425-441.
  6. Sandström, J. P., J. A. Russell, J. P. White, and N. A. Moran. 2001.  Independent origins and horizontal transfer of bacterial symbionts of aphids. Molecular Ecology 10: 217-228.
  7. Mira, A., H. Ochman and N. A. Moran. 2001. Deletional bias and the evolution of bacterial genomes. Trends in Genetics 17: 589-596.
  8. Moran, N. A. and A. Mira. 2001. The process of genome shrinkage in the obligate symbiont, Buchnera aphidicola. Genome Biology 2: research0054.1-0054.12.
  9. Moran, N. A. 2002. The ubiquitous and varied role of infection in the lives of animals and plants. The American Naturalist 160:S1-S8.
  10. Tamas, I., Klasson, L., Näslund, K., Canbäck, B.,  Eriksson, A.-S., Wernegreen J. J., Sandström, J. P., Moran, N. A.,  and S. G. E. Andersson. 2002. Fifty million years of genomic stasis in endosymbiotic bacteria. Science 296: 2376-2379.
  11. Oliver, K., J. Russell, N. Moran and M. Hunter. 2003. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proceedings of the National Academy of Sciences USA 100: 1803-1807.
  12. Lerat, E., V. Daubin and N. A. Moran. 2003. From gene trees to organismal phylogeny in prokaryotes: the case of the g-Proteobacteria. PLoS- Biology 1: 101-108.
  13. Moran, N. A., J. A. Russell, T. Fukatsu and R. Koga. 2005. Evolutionary relationships of three new species of Enterobacteriaceae living as symbionts of aphids and other insects. Applied and Environmental Microbiology 71: 3302-3310.
  14. Moran, N. A., H. E. Dunbar and J. L. Wilcox. 2005. Regulation of transcription in a reduced bacterial genome: nutrient-provisioning genes of the obligate symbiont, Buchnera aphidicola.  Journal of Bacteriology 187: 4229-4237.
  15. Oliver, K. M., N. A. Moran and M. S. Hunter. 2005. Variation in resistance to parasitism in aphids is due to symbionts and not host genotype. Proceedings of the National Academy of Sciences USA 102: 12975-12800.
  16. Moran, N. A., P. Tran and N. M. Gerardo. 2005. Symbiosis and insect diversification: an ancient symbiont of sap-feeding insects from the bacterial phylum Bacteroidetes. Applied and Environmental Microbiology 71: 8802-8810.
  17. Wu, D., S. C. Daugherty, S. E. Van Aken, G. H. Pai, K. L. Watkins, H. Khouri, L. J. Tallon, J. M. Zaborsky, H. E. Dunbar, P. L. Tran, N. A. Moran and J. A. Eisen. 2006. Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters. PLoS Biology 4: e188.
  18. Nakabachi, A., A. Yamashita, H. Toh, H. Ishikawa, H. E. Dunbar, N. A. Moran and M. Hattori. 2006. The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science 314: 267.
  19. Russell, J. A. and N. A. Moran. 2006. Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proceedings of the Royal Society B: Biological Sciences 273: 603-610.
  20. Moran, N. A. and H. E. Dunbar. 2006. Sexual acquisition of beneficial symbionts in aphids. Proceedings of the National Academy of Sciences USA 103: 12803-12806.
  21. McCutcheon, J. M. and N. A. Moran. 2007. Parallel genomic evolution and metabolic interdependence in an ancient symbiosis. Proceedings of the National Academy of Sciences USA 104: 19392-19397.
  22. Dunbar, H. E., A. C. C. Wilson, N. R. Ferguson and N. A. Moran. 2007. Aphid thermal tolerance is governed by a point mutation in bacterial symbionts. PLoS Biology 5: e96.
  23. Moran, N. A., H. J. McLaughlin, and R. Sorek. 2009. The dynamics and timescale of ongoing genomic erosion in symbiotic bacteria. Science 323: 379-382.
  24. Degnan, P.H., Y. Yu, N. Sisneros, R. A. Wing, and N. A. Moran. 2009. Hamiltonella defensa, genome evolution of a protective bacterial endosymbiont from pathogenic ancestors. Proceedings of the National Academy of Sciences USA 106: 9063-9068.
  25. McCutcheon, J. M., B. R. MacDonald, and N. A. Moran. 2009. Origin of an alternative genetic code in the extremely small and GC-rich genome of a bacterial symbiont. PLoS-Genetics 5: e1000565.
  26. Peccoud, J., J. C. Simon, H. J. McLaughlin, and N. A. Moran. 2009. Recent adaptive radiation of pea aphids revealed by their rapidly evolving symbionts. Proceedings of the National Academy of Sciences USA 106: 16315-16320.
  27. Oliver, K. M., P. H. Degnan, M. S. Hunter, and N. A. Moran. 2009. Bacteriophage encode factors required for protection in a symbiotic mutualism. Science 325: 992-994.
  28. McCutcheon, J. M., B. R. MacDonald, and N. A. Moran. 2009. Convergent evolution of metabolic roles in bacterial co-symbionts of insects. Proceedings of the National Academy of Sciences USA 106:15394-15399.
  29. Sabree, Z. L., Kambhampati, S., and N. A. Moran. 2009. Nitrogen recycling and nutritional provisioning by the cockroach endosymbiont, Blattabacterium. Proceedings of the National Academy of Sciences USA 106:19521-19516.
  30. Degnan, P. H., T. E. Leonardo, B. N. Cass, B. Hurwitz, D. Stern, R. A. Gibbs, S. Richards and N. A. Moran. 2010. Dynamics of genome evolution in facultative symbionts of aphids. Environmental Microbiology 12: 2060-2069.
  31. Moran, N. A. and T. Jarvik. 2010. Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science 328: 624-627.