Joseph Bondy-Denomy, PhD

Associate Professor
Microbiology and Immunology
[email protected]
+1 415 514-1381

In the Bondy-Denomy lab, we study CRISPR-Cas bacterial immune systems in an effort to understand their role in antagonizing viruses called bacteriophages. We are very interested in how CRISPR works and the ways that phages inhibit and evade CRISPR-Cas function.

Publications: 

Single phage proteins sequester signals from TIR and cGAS-like enzymes.

Nature

Li D, Xiao Y, Fedorova I, Xiong W, Wang Y, Liu X, Huiting E, Ren J, Gao Z, Zhao X, Cao X, Zhang Y, Bondy-Denomy J, Feng Y

Diverse viral cas genes antagonize CRISPR immunity.

Nature

Katz MA, Sawyer EM, Oriolt L, Kozlova A, Williams MC, Margolis SR, Johnson M, Bondy-Denomy J, Meeske AJ

AcrIF11 is a potent CRISPR-specific ADP-ribosyltransferase encoded by phage and plasmid.

bioRxiv : the preprint server for biology

Chen DF, Roe LT, Li Y, Borges AL, Zhang JY, Babbar P, Maji S, Stevens MGV, Correy GJ, Diolaiti ME, Smith DH, Ashworth A, Stroud RM, Kelly MJS, Bondy-Denomy J, Fraser JS

Exploring the diversity of anti-defense systems across prokaryotes, phages, and mobile genetic elements.

bioRxiv : the preprint server for biology

Tesson F, Huiting E, Wei L, Ren J, Johnson MC, Planel R, Cury J, Feng Y, Bondy-Denomy J, Bernheim A

Characterization of a lipid-based jumbo phage compartment as a hub for early phage infection.

Cell host & microbe

Mozumdar D, Fossati A, Stevenson E, Guan J, Nieweglowska E, Rao S, Agard D, Swaney DL, Bondy-Denomy J

Anti-CRISPR proteins trigger a burst of CRISPR-Cas9 expression that enhances phage defense.

Cell reports

Workman RE, Stoltzfus MJ, Keith NC, Euler CW, Bondy-Denomy J, Modell JW

Phage anti-CBASS protein simultaneously sequesters cyclic trinucleotides and dinucleotides.

Molecular cell

Cao X, Xiao Y, Huiting E, Cao X, Li D, Ren J, Fedorova I, Wang H, Guan L, Wang Y, Li L, Bondy-Denomy J, Feng Y

Cas9 degradation in human cells using phage anti-CRISPR proteins.

PLoS biology

Meacham Z, de Tacca LA, Bondy-Denomy J, Rabuka D, Schelle M

Identification of an anti-CRISPR protein that inhibits the CRISPR-Cas type I-B system in Clostridioides difficile.

mSphere

Muzyukina P, Shkaruta A, Guzman NM, Andreani J, Borges AL, Bondy-Denomy J, Maikova A, Semenova E, Severinov K, Soutourina O

Single phage proteins sequester TIR- and cGAS-generated signaling molecules.

bioRxiv : the preprint server for biology

Li D, Xiao Y, Xiong W, Fedorova I, Wang Y, Liu X, Huiting E, Ren J, Gao Z, Zhao X, Cao X, Zhang Y, Bondy-Denomy J, Feng Y

Next-generation proteomics for quantitative Jumbophage-bacteria interaction mapping.

Nature communications

Fossati A, Mozumdar D, Kokontis C, Mèndez-Moran M, Nieweglowska E, Pelin A, Li Y, Guo B, Krogan NJ, Agard DA, Bondy-Denomy J, Swaney DL

Core defense hotspots within Pseudomonas aeruginosa are a consistent and rich source of anti-phage defense systems.

Nucleic acids research

Johnson MC, Laderman E, Huiting E, Zhang C, Davidson A, Bondy-Denomy J

F-Type Pyocins Are Diverse Noncontractile Phage Tail-Like Weapons for Killing Pseudomonas aeruginosa.

Journal of bacteriology

Saha S, Ojobor CD, Li ASC, Mackinnon E, North OI, Bondy-Denomy J, Lam JS, Ensminger AW, Maxwell KL, Davidson AR

Phage anti-CBASS protein simultaneously sequesters cyclic trinucleotides and dinucleotides.

bioRxiv : the preprint server for biology

Cao X, Xiao Y, Huiting E, Cao X, Li D, Ren J, Guan L, Wang Y, Li L, Bondy-Denomy J, Feng Y

Defining the expanding mechanisms of phage-mediated activation of bacterial immunity.

Current opinion in microbiology

Huiting E, Bondy-Denomy J

Ten Years of Anti-CRISPR Research.

Journal of molecular biology

Bondy-Denomy J, Maxwell KL, Davidson AR

Next-generation interaction proteomics for quantitative Jumbophage-bacteria interaction mapping.

bioRxiv : the preprint server for biology

Fossati A, Mozumdar D, Kokontis C, Mèndez-Moran M, Nieweglowska E, Pelin A, Li Y, Guo B, Krogan NJ, Agard DA, Bondy-Denomy J, Swaney DL

The ϕPA3 phage nucleus is enclosed by a self-assembling 2D crystalline lattice.

Nature communications

Nieweglowska ES, Brilot AF, Méndez-Moran M, Kokontis C, Baek M, Li J, Cheng Y, Baker D, Bondy-Denomy J, Agard DA

Bacteriophages inhibit and evade cGAS-like immune function in bacteria.

Cell

Huiting E, Cao X, Ren J, Athukoralage JS, Luo Z, Silas S, An N, Carion H, Zhou Y, Fraser JS, Feng Y, Bondy-Denomy J

Bacteriophage genome engineering with CRISPR-Cas13a.

Nature microbiology

Guan J, Oromí-Bosch A, Mendoza SD, Karambelkar S, Berry JD, Bondy-Denomy J

Structural basis of AcrIF24 as an anti-CRISPR protein and transcriptional suppressor.

Nature chemical biology

Mukherjee IA, Gabel C, Noinaj N, Bondy-Denomy J, Chang L

CRISPR-Cas12a targeting of ssDNA plays no detectable role in immunity.

Nucleic acids research

Marino ND, Pinilla-Redondo R, Bondy-Denomy J

Lack of Cas13a inhibition by anti-CRISPR proteins from Leptotrichia prophages.

Molecular cell

Johnson MC, Hille LT, Kleinstiver BP, Meeske AJ, Bondy-Denomy J

A single bacterial enzyme i(NHI)bits phage DNA replication.

Cell host & microbe

Huiting E, Bondy-Denomy J

Distinct Subcellular Localization of a Type I CRISPR Complex and the Cas3 Nuclease in Bacteria.

Journal of bacteriology

Govindarajan S, Borges A, Karambelkar S, Bondy-Denomy J

Genetic Manipulation of a CAST of Characters in a Microbial Community.

The CRISPR journal

Mozumdar D, Csörgo B, Bondy-Denomy J

CRISPR inactivation by integration.

Nature microbiology

Bondy-Denomy J

Positioning Diverse Type IV Structures and Functions Within Class 1 CRISPR-Cas Systems.

Frontiers in microbiology

Taylor HN, Laderman E, Armbrust M, Hallmark T, Keiser D, Bondy-Denomy J, Jackson RN

Mobile element warfare via CRISPR and anti-CRISPR in Pseudomonas aeruginosa.

Nucleic acids research

León LM, Park AE, Borges AL, Zhang JY, Bondy-Denomy J

A phage-encoded anti-activator inhibits quorum sensing in Pseudomonas aeruginosa.

Molecular cell

Shah M, Taylor VL, Bona D, Tsao Y, Stanley SY, Pimentel-Elardo SM, McCallum M, Bondy-Denomy J, Howell PL, Nodwell JR, Davidson AR, Moraes TF, Maxwell KL

Intracellular Organization by Jumbo Bacteriophages.

Journal of bacteriology

Guan J, Bondy-Denomy J

Discovery of multiple anti-CRISPRs highlights anti-defense gene clustering in mobile genetic elements.

Nature communications

Pinilla-Redondo R, Shehreen S, Marino ND, Fagerlund RD, Brown CM, Sørensen SJ, Fineran PC, Bondy-Denomy J

A compact Cascade-Cas3 system for targeted genome engineering.

Nature methods

Csörgo B, León LM, Chau-Ly IJ, Vasquez-Rifo A, Berry JD, Mahendra C, Crawford ED, Lewis JD, Bondy-Denomy J

Machine-learning approach expands the repertoire of anti-CRISPR protein families.

Nature communications

Gussow AB, Park AE, Borges AL, Shmakov SA, Makarova KS, Wolf YI, Bondy-Denomy J, Koonin EV

Structures and Strategies of Anti-CRISPR-Mediated Immune Suppression.

Annual review of microbiology

Wiegand T, Karambelkar S, Bondy-Denomy J, Wiedenheft B

Author Correction: Broad-spectrum anti-CRISPR proteins facilitate horizontal gene transfer.

Nature microbiology

Mahendra C, Christie KA, Osuna BA, Pinilla-Redondo R, Kleinstiver BP, Bondy-Denomy J

Critical Anti-CRISPR Locus Repression by a Bi-functional Cas9 Inhibitor.

Cell host & microbe

Osuna BA, Karambelkar S, Mahendra C, Sarbach A, Johnson MC, Kilcher S, Bondy-Denomy J

Listeria Phages Induce Cas9 Degradation to Protect Lysogenic Genomes.

Cell host & microbe

Osuna BA, Karambelkar S, Mahendra C, Christie KA, Garcia B, Davidson AR, Kleinstiver BP, Kilcher S, Bondy-Denomy J

Broad-spectrum anti-CRISPR proteins facilitate horizontal gene transfer.

Nature microbiology

Mahendra C, Christie KA, Osuna BA, Pinilla-Redondo R, Kleinstiver BP, Bondy-Denomy J

Bacterial alginate regulators and phage homologs repress CRISPR-Cas immunity.

Nature microbiology

Borges AL, Castro B, Govindarajan S, Solvik T, Escalante V, Bondy-Denomy J

Anti-CRISPR protein applications: natural brakes for CRISPR-Cas technologies.

Nature methods

Marino ND, Pinilla-Redondo R, Csörgo B, Bondy-Denomy J

Author Correction: Cryptic inoviruses revealed as pervasive in bacteria and archaea across Earth's biomes.

Nature microbiology

Roux S, Krupovic M, Daly RA, Borges AL, Nayfach S, Schulz F, Sharrar A, Matheus Carnevali PB, Cheng JF, Ivanova NN, Bondy-Denomy J, Wrighton KC, Woyke T, Visel A, Kyrpides NC, Eloe-Fadrosh EA

A bacteriophage nucleus-like compartment shields DNA from CRISPR nucleases.

Nature

Mendoza SD, Nieweglowska ES, Govindarajan S, Leon LM, Berry JD, Tiwari A, Chaikeeratisak V, Pogliano J, Agard DA, Bondy-Denomy J

A Type IV-A CRISPR-Cas System in Pseudomonas aeruginosa Mediates RNA-Guided Plasmid Interference In Vivo.

The CRISPR journal

Crowley VM, Catching A, Taylor HN, Borges AL, Metcalf J, Bondy-Denomy J, Jackson RN

Molecular mechanism of azithromycin resistance among typhoidal Salmonella strains in Bangladesh identified through passive pediatric surveillance.

PLoS neglected tropical diseases

Hooda Y, Sajib MSI, Rahman H, Luby SP, Bondy-Denomy J, Santosham M, Andrews JR, Saha SK, Saha S

CRISPR-Cas System of a Prevalent Human Gut Bacterium Reveals Hyper-targeting against Phages in a Human Virome Catalog.

Cell host & microbe

Soto-Perez P, Bisanz JE, Berry JD, Lam KN, Bondy-Denomy J, Turnbaugh PJ

Anti-CRISPR-Associated Proteins Are Crucial Repressors of Anti-CRISPR Transcription.

Cell

Stanley SY, Borges AL, Chen KH, Swaney DL, Krogan NJ, Bondy-Denomy J, Davidson AR

Cryptic inoviruses revealed as pervasive in bacteria and archaea across Earth's biomes.

Nature microbiology

Roux S, Krupovic M, Daly RA, Borges AL, Nayfach S, Schulz F, Sharrar A, Matheus Carnevali PB, Cheng JF, Ivanova NN, Bondy-Denomy J, Wrighton KC, Woyke T, Visel A, Kyrpides NC, Eloe-Fadrosh EA

Cas13 Helps Bacteria Play Dead when the Enemy Strikes.

Cell host & microbe

Mendoza SD, Bondy-Denomy J

Anti-CRISPR-mediated control of gene editing and synthetic circuits in eukaryotic cells.

Nature communications

Nakamura M, Srinivasan P, Chavez M, Carter MA, Dominguez AA, La Russa M, Lau MB, Abbott TR, Xu X, Zhao D, Gao Y, Kipniss NH, Smolke CD, Bondy-Denomy J, Qi LS

Temperature-Responsive Competitive Inhibition of CRISPR-Cas9.

Molecular cell

Jiang F, Liu JJ, Osuna BA, Xu M, Berry JD, Rauch BJ, Nogales E, Bondy-Denomy J, Doudna JA

Phage Morons Play an Important Role in Pseudomonas aeruginosa Phenotypes.

Journal of bacteriology

Tsao YF, Taylor VL, Kala S, Bondy-Denomy J, Khan AN, Bona D, Cattoir V, Lory S, Davidson AR, Maxwell KL

A Unified Resource for Tracking Anti-CRISPR Names.

The CRISPR journal

Bondy-Denomy J, Davidson AR, Doudna JA, Fineran PC, Maxwell KL, Moineau S, Peng X, Sontheimer EJ, Wiedenheft B

Discovery of widespread type I and type V CRISPR-Cas inhibitors.

Science (New York, N.Y.)

Marino ND, Zhang JY, Borges AL, Sousa AA, Leon LM, Rauch BJ, Walton RT, Berry JD, Joung JK, Kleinstiver BP, Bondy-Denomy J

Bacteriophage Cooperation Suppresses CRISPR-Cas3 and Cas9 Immunity.

Cell

Borges AL, Zhang JY, Rollins MF, Osuna BA, Wiedenheft B, Bondy-Denomy J

Protein Inhibitors of CRISPR-Cas9.

ACS chemical biology

Bondy-Denomy J

How bacteria control the CRISPR-Cas arsenal.

Current opinion in microbiology

Leon LM, Mendoza SD, Bondy-Denomy J

Pseudomonas aeruginosa defends against phages through type IV pilus glycosylation.

Nature microbiology

Harvey H, Bondy-Denomy J, Marquis H, Sztanko KM, Davidson AR, Burrows LL

The Discovery, Mechanisms, and Evolutionary Impact of Anti-CRISPRs.

Annual review of virology

Borges AL, Davidson AR, Bondy-Denomy J

Disabling Cas9 by an anti-CRISPR DNA mimic.

Science advances

Shin J, Jiang F, Liu JJ, Bray NL, Rauch BJ, Baik SH, Nogales E, Bondy-Denomy J, Corn JE, Doudna JA

Cas1 and the Csy complex are opposing regulators of Cas2/3 nuclease activity.

Proceedings of the National Academy of Sciences of the United States of America

Rollins MF, Chowdhury S, Carter J, Golden SM, Wilkinson RA, Bondy-Denomy J, Lander GC, Wiedenheft B

Structure Reveals Mechanisms of Viral Suppressors that Intercept a CRISPR RNA-Guided Surveillance Complex.

Cell

Chowdhury S, Carter J, Rollins MF, Golden SM, Jackson RN, Hoffmann C, Nosaka L, Bondy-Denomy J, Maxwell KL, Davidson AR, Fischer ER, Lander GC, Wiedenheft B

CRISPR control of virulence in Pseudomonas aeruginosa.

Cell research

Wiedenheft B, Bondy-Denomy J

Inhibition of CRISPR-Cas9 with Bacteriophage Proteins.

Cell

Rauch BJ, Silvis MR, Hultquist JF, Waters CS, McGregor MJ, Krogan NJ, Bondy-Denomy J

Quorum sensing controls the Pseudomonas aeruginosa CRISPR-Cas adaptive immune system.

Proceedings of the National Academy of Sciences of the United States of America

Høyland-Kroghsbo NM, Paczkowski J, Mukherjee S, Broniewski J, Westra E, Bondy-Denomy J, Bassler BL

The solution structure of an anti-CRISPR protein.

Nature communications

Maxwell KL, Garcia B, Bondy-Denomy J, Bona D, Hidalgo-Reyes Y, Davidson AR

Prophages mediate defense against phage infection through diverse mechanisms.

The ISME journal

Bondy-Denomy J, Qian J, Westra ER, Buckling A, Guttman DS, Davidson AR, Maxwell KL

The diversity-generating benefits of a prokaryotic adaptive immune system.

Nature

van Houte S, Ekroth AK, Broniewski JM, Chabas H, Ashby B, Bondy-Denomy J, Gandon S, Boots M, Paterson S, Buckling A, Westra ER

Active and adaptive Legionella CRISPR-Cas reveals a recurrent challenge to the pathogen.

Cellular microbiology

Rao C, Guyard C, Pelaz C, Wasserscheid J, Bondy-Denomy J, Dewar K, Ensminger AW

Foreign DNA acquisition by the I-F CRISPR-Cas system requires all components of the interference machinery.

Nucleic acids research

Vorontsova D, Datsenko KA, Medvedeva S, Bondy-Denomy J, Savitskaya EE, Pougach K, Logacheva M, Wiedenheft B, Davidson AR, Severinov K, Semenova E

Multiple mechanisms for CRISPR-Cas inhibition by anti-CRISPR proteins.

Nature

Bondy-Denomy J, Garcia B, Strum S, Du M, Rollins MF, Hidalgo-Reyes Y, Wiedenheft B, Maxwell KL, Davidson AR

Parasite Exposure Drives Selective Evolution of Constitutive versus Inducible Defense.

Current biology : CB

Westra ER, van Houte S, Oyesiku-Blakemore S, Makin B, Broniewski JM, Best A, Bondy-Denomy J, Davidson A, Boots M, Buckling A

When a virus is not a parasite: the beneficial effects of prophages on bacterial fitness.

Journal of microbiology (Seoul, Korea)

Bondy-Denomy J, Davidson AR

To acquire or resist: the complex biological effects of CRISPR-Cas systems.

Trends in microbiology

Bondy-Denomy J, Davidson AR

Bacteriophage genes that inactivate the CRISPR/Cas bacterial immune system.

Nature

Bondy-Denomy J, Pawluk A, Maxwell KL, Davidson AR

Efficacy of bacteriophage treatment on Pseudomonas aeruginosa biofilms.

Journal of endodontics

Phee A, Bondy-Denomy J, Kishen A, Basrani B, Azarpazhooh A, Maxwell K

The CRISPR/Cas adaptive immune system of Pseudomonas aeruginosa mediates resistance to naturally occurring and engineered phages.

Journal of bacteriology

Cady KC, Bondy-Denomy J, Heussler GE, Davidson AR, O'Toole GA

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