Rice University
BioSciences at Rice

Yousif Shamoo

Professor of BioSciences

Our interest in molecular evolution is stimulated by the rise in drug resistant pathogens and how understanding the physical basis for adaptation can be used for prediction of resistance and the identification of new targets and strategies for antimicrobial therapies. By combining approaches from biophysics and experimental evolution we are able to identify and characterize intermediates along the mutational pathways of adaptation and then link those intermediates to the overall evolutionary trajectory of the bacterial populations. Adaptive changes in protein sequence and expression impact organismal fitness and, consequently, dictate population dynamics. By combining experimental evolution with molecular biophysics we take a systems level view of adaptation and link it to the molecular mechanism responsible for the resulting evolutionary dynamics.

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Reyes J, Panesso D, Tran TT, Mishra NN, Cruz MR, Munita JM, Singh KV, Yeaman MR, Murray BE, Shamoo Y, Garsin D, Bayer AS, Arias CA.  A liaR deletion restores susceptibility to daptomycin and antimicrobial peptides in multidrug-resistant Enterococcus faecalis. The Journal of infectious diseases. 2015; 211(8):1317-25. PMCID: PMC4402337

Beabout K, Hammerstrom TG, Perez A, Magalhães B, Prater A, Clements T, Arias C, Saxer G, Shamoo Y. The ribosomal S10 protein is a general target for decreased tigecycline susceptibility. Antimicrob Agents Chemother. 2015.  59(9):5561-5566 PMCID: PMC4538488 

Diaz L, Tran TT, Munita JM, Miller WR, Rincon S, Carvajal LP, Wollam A, Reyes J, Panesso D, Rojas NL, Shamoo Y, Murray BE, Weinstock GM, Arias CA Whole-genome analyses of Enterococcus faecium isolates with diverse daptomycin MICs.  Antimicrob Agents Chemother., 58(8 2014: 4527-34

Saxer G, Krepps MD, Merkley ED, Ansong C, Deatherage Kaiser BL, Valovska MT, Ristic N, Yeh PT, Prakash VP, Leiser OP, Nakhleh L, Gibbons HS, Kreuzer HW, Shamoo Y. Mutations in global regulators lead to metabolic selection during adaptation to complex environments..  PLoS Genet., 10(12) 2014: :e1004872

Davlieva M, Donarski J, Wang J, Shamoo Y, Nikonowicz EP. Structure analysis of free and bound states of an RNA aptamer against ribosomal protein S8 from Bacillus anthracis.  Nucleic Acids Res., 42(16) 2014: 10795-808

Nicolaou KC, Hale CR, Nilewski C, Ioannidou HA, ElMarrouni A, Nilewski LG, Beabout K, Wang TT, Shamoo Y. Total synthesis of viridicatumtoxin B and analogues thereof: strategy evolution, structural revision, and biological evaluation .   J Am Chem Soc., 136(34) 2014: 12137-60

Miller C, Kong J, Tran TT, Arias CA, Saxer G, Shamoo Y. Adaptation of Enterococcus faecalis to daptomycin reveals an ordered progression to resistance.  Antimicrob Agents Chemother, 57(11) 2013: 5373-83

Davlieva M, Zhang W, Arias CA, Shamoo Y. Biochemical characterization of cardiolipin synthase mutations associated with daptomycin resistance in enterococci.  Antimicrob Agents Chemother, 57(1) 2013: 289-96

Tran TT, Panesso D, Mishra NN, Mileykovskaya E, Guan Z, Munita JM, Reyes J, Diaz L, Weinstock GM, Murray BE, Shamoo Y, Dowhan W, Bayer AS, Arias CA. Daptomycin-resistant Enterococcus faecalis diverts the antibiotic molecule from the division septum and remodels cell membrane phospholipids.  MBio, 4(4) 2013: e00281-13

Agrawal A, Chipara AC, Shamoo Y, Patra PK, Carey BJ, Ajayan PM, Chapman WG, Verduzco R. Dynamic self-stiffening in liquid crystal elastomers.  Nat Commun, 4 2013: 1739

Tran TT, Panesso D, Gao H, Roh JH, Munita JM, Reyes J, Diaz L, Lobos EA, Shamoo Y, Mishra NN, Bayer AS, Murray BE, Weinstock GM, Arias CA. Whole-Genome Analysis of a Daptomycin-Susceptible Enterococcus faecium Strain and Its Daptomycin-Resistant Variant Arising during Therapy.  Antimicrob Agents Chemother, 57(1) 2013: 261-8

Mishra NN, Bayer AS, Tran TT, Shamoo Y, Mileykovskaya E, Dowhan W, Guan Z, Arias CA. Daptomycin resistance in enterococci is associated with distinct alterations of cell membrane phospholipid content.  PLoS One, 7(8) 2012: e43958

Arias, C.A., McGrath, D., Qin, X.,Mojica M.F., Miller C., Diaz S. L., Tran, T.T., Rincon, S., Barbu, E.M., Reyes, J.C., Panesso, D., Lobos, E., Sodergren, E., Pasqualini, R., Arap, W., Quinn, J.P., Shamoo, Y., Murray, B.E., and Weinstock, G. Whole-Genome and Cell Envelope Analysis of Daptomycin- Susceptible Enterococcus faecalis and Its Resistant Derivative that Arose During Therapy.  New Engl. J. Med., 362 2011: 892-900. PMID 21899450

Walkiewicz K., Lau K. and Shamoo Y. Biophysical basis for TetX mediated antibiotic resistance.   2010

Davilieva, M. and Shamoo, Y. Crystal structure of a trimeric archaeal adenylate kinase from the mesophile Methanococcus maripaludis with an unusually broad functional range and thermal stability.  Proteins, 78 2010: 357-364

Miller C. and Shamoo Y. Experimental Evolution of Daptomycin Resistance in Enterococcus Faecalis.   2010

Miller, C., Davilieva, M., Wilson, C., White, K., Counago, R., Wu, G., Myers, J.C., Wittung-Stafshede, P., and Shamoo, Y. Experimental evolution of adenylate kinase reveals contrasting strategies towards protein thermostability.  Biophys. J, 99 2010: 887-896 PMID: 20682267

Peña M., Davlieva M., Bennett M.R., Olson J.S. and Shamoo Y. Protein folding dynamics and function determine evolutionary fates in a microbial population.   2010

Davlieva M., Doneske J., Michnicka M., Nikonowicz E. and Shamoo Y. Structural studies of an RNA aptamer with high affinity for the B. anthracis ribosomal protein S8.   2010

Guelker, M., Stagg, L., Wittung-Stafshede, P., and Shamoo, Y. Pseudo symmetry, high copy number and twinning complicate the structure determination of flavodoxin from Desulfovibrio desulfuricans (ATCC 29577).  Acta Cryst D Biol Crystallogr, D65 2009: 513-522

Davlieva, M. and Shamoo, Y. Structure and biochemical characterization of an adenylate kinase originating from the psychrophilic organism Marinibacillus marinus .  Acta Cryst F Struc Biol Cryst Commun, 65 2009: 751-756

Couñago, R., Wilson, C.J., Peña, M.I., Wittung-Stafshede, P., and Shamoo, Y. An adaptive mutation in adenylate kinase that increases organismal fitness is linked to stability-activity trade-offs.  Prot. Eng. Des. Sel., 21 2008: 19-27

Woodward, A.W., Ratzel, S.E., Woodward, E.E., Shamoo, Y., and Bartel, B. Mutation of E1-CONJUGATING ENZYME-RELATED1 decreases RELATED TO UBIQUITIN conjugation and alters auxin response and development.  Plant Physiology, 144 2007: 976-987

Counago, R., Chen, S. and Shamoo, Y. In vivo evolution reveals biophysical origins of organismal fitness.  Molecular Cell, 22 2006: 441-446

Brock, D.A., van Egmond, W.N., Shamoo. Y., Hatton, R.D., and Gomer, R.H. A 60-kilodalton protein component of the counting factor regulates group size in Dictyostelium discoideum.  Eularyotic Cell, 5 2006: 1532-1538

Maximciuc, A., Putkey, J.A., Shamoo, Y., and Mackenzie, K.R. Complex of calmodulin with a ryanodine receptor target reveals a novel, flexible binding mode.  Structure, 14 2006: 1547-1556

Sun, S., Geng, L., and Shamoo, Y. Fusion of bacteriophage RB69 DNA polymerase and single-stranded DNA binding protein leads to increased processivity.  Prot. Struc. Func. and Bioinform., 65 2006: 231-238

Morozova, N., Aller, J.A., Myers, J., and Shamoo, Y. Protein-RNA interactions: Exploring binding patterns with a three-dimensional superposition analysis of high resolution structures.  Bioinformatics, 22 2006: 2746-2752

Counago, R., and Shamoo, Y. Gene replacement of adenylate kinase in the gram-positive thermophile Geobacillus stearothermophilus disrupts adenine nucleotide homeostasis and reduces cell viability.  Extremophiles, 9 2005: 135-144

Myers, J., and Shamoo, Y. Human UP1 as a model for understanding purine recognition in the family of proteins containing the RNA Recognition Motif (RRM).  J. Mol. Biol., 342 2004: 743-756

Bruning, J.B., and Shamoo, Y. Structural and thermodynamic analysis of human PCNA bound to peptides derived from DNA polymerase-delta p66-subunit and flap endonuclease-1 (FEN1) proteins.  Structure 2004In Press

Sun, S., and Shamoo, Y. Biochemical characterization of interactions between DNA polymerase and single-stranded DNA binding protein in bacteriophage RB69.  J. Biol. Chem., 278 2003: 3876-3881

Shamoo, Y. Structural insights into BRCA2 function.  Curr. Op. Struc. Biol., 13 2003: 206-211

Myers, J.G., Moore, S.A., and Shamoo, Y. Structure-based incorporation of 6-MI into the human telomeric repeat DNA as a probe for UP1 binding and destabilization of G-tetrad structures.  J. Biol. Chem., 278 2003: 42300-42306

Allers, J., and Shamoo, Y. Structure-based analysis of protein-RNA interactions using the program ENTANGLE.  J. Mol. Biol., 311 2001: 76-86

Shamoo, Y. Single-stranded DNA Binding Proteins.  in Encyclopedia of Life Sciences 2000

Shamoo, Y., and Steitz, T.A. Building a Replisome Structure from Interacting Pieces: Structures of a Sliding Clamp Complexed with an Interaction Peptide from DNA Polymerase, and a DNA Polymerase Editing Complex.  Cell, 99 1999: 155-169

Rice, L.M., Shamoo, Y., and Brunger, A.T Phase Improvement by Multi-start Simulated Annealing Refinement and Structure Factor Averaging.  J. Appl. Cryst., 31 1998: 798-805

Walkiewicz K, Benitez Cardenas AS, Sun C, Bacorn C, Saxer G, Shamoo Y. Small changes in enzyme function can lead to surprisingly large fitness effects during adaptive evolution of antibiotic resistance.  Proc Natl Acad Sci U S A., 109(52) 2012 Dec 26: 21408-13

Panesso D, Reyes J, Gaston EP, Deal M, Londoño A, Nigo M, Munita JM, Miller WR, Shamoo Y, Tran TT, Arias CA. Deletion of liaR reverses eaptomycin resistance in Enterococcus faecium independent of the genetic background. Antimicrob Agents Chemother. 2015. 59(12):7327-34. PMCID: PMC4649183 [Available on 2016-06-01]

Hammerstrom TG, Beabout K, Clements TP, Saxer G, Shamoo Y. Acinetobacter baumannii repeatedly evolves a hypermutator phenotype in response to tigecycline that effectively surveys evolutionary trajectories to resistance. PLoS One 2015. 10(10):e0140489. PMCID: PMC4619398  

Shamoo Lab

  • B.S. Biology (1983) Carnegie-Mellon University
  • Ph.D. Molecular Biophysics and Biochemistry (1988) Yale University
  • Institute of Biosciences and Bioengineering
  • Keck Center for Quantitative Biomedical Sciences
  • Ken Kennedy Institute for Information Technology
Research Areas
  • Structural biology, molecular evolution, X-ray crystallography, microbial evolution, antibiotic resistance
Professional Experience
  • Associate Professor in Ecol & Evol. Biol.
    Rice University
    09/2010-present
  • Associate Professor in Biochem. & Cell Biol.
    Rice University
    2005-present
  • Director- Institute of Biosciences and Bioengineering
    Rice University
  • Post-doctoral Associate/Fellow
    Yale University
    1989-1992
  • Associate Research Scientist
    Yale University
    1993-1998
  • Assistant Professor
    Rice University
    1998-2005
Contact Information
Email: shamoo@rice.edu
Phone: 713-348-5493
Office: Keck Hall, 332