Efrem Lim
Biography
Efrem Lim is a virologist who studies the human virome in health and disease. The virome is the diverse community of viruses harbored in and on humans, some of which cause disease while others are commensal. The Lim lab is particularly interested in understanding the interactions of the human virome in development and immunity. While most microbiome studies focus on bacteria, his interdisciplinary group sheds light on how viruses shape host-microbiome interactions.
The Lim lab integrates molecular virology and bioinformatics approaches in clinical cohorts to understand:
- how the virome impacts the trajectory of infant development
- the role of microbiome interactions in disease
Their research is being used in precision medicine that personalizes the prevention and treatment of diseases to individuals.
In response to the COVID-19 pandemic, the Lim lab has led research efforts to understand and prevent SARS-CoV-2 transmission. This includes next-generation sequencing studies of SARS-CoV-2 to identify transmission patterns and functional studies to characterize virus mutations in clinical isolates.
- Next-generation sequencing characterization of SARS-CoV-2 genomes from sentinel surveillance in Tempe, Arizona early in the pandemic (Jan-Mar 2020).
- Phylodynamic tracing to provide unique epidemiological insights into the origins and transmission of SARS-CoV-2 in Arizona, in a joint state-wide effort called the Arizona COVID-19 Genomics Union (ACGU).
- Confirmation of the first B.1.1.7/UK variant cases in Arizona. The 3 genome sequences clade within 20I/501Y.V1, also known as B.1.1.7 lineage or the “UK variant”. Samples were sequenced twice, independently.
- Genomic sequencing surveillance identification of a new E484K variant of interest in Arizona called B.1.243.1. This variant is being established in Arizona, but there is now evidence of transmission to other states in the US. 21 out of 24 cases of B.1.243.1 are from Arizona beginning in early February. The other 3 cases have been reported in Texas and New Mexico.
- Establishment of the ASU COVID-19 Sequencing Center. We continue to track variants of concern in real-time using next-generation sequencing. This information is used to inform public health responses and policies. We have sequenced more than 4,000 COVID-19 cases.
Education
PhD, University of Washington
Research Interests
Virome, Microbiome, SARS-CoV-2
Publications
- Skidmore PT, Kaelin EA, Holland LA, Maqsood R, Wu LI, Mellor NJ, Blain JM, Harris V, LaBaer J, Murugan V, Lim ES. (2021) Genomic Sequencing Surveillance Identifies Emergence of SARS-CoV-2 E484K variant B.1.243.1 in Arizona. Emerging Infectious Diseases. In Press. Preprint medRxiv.
- Saha P, Skidmore PT, Holland LA, Mondal A, Bose D, Seth R, Sullivan K, Janulewicz P, Horner R, Klimas N, Nagarkatti M, Nagarkatti P, Lim ES, Chatterjee S. (2021) Andrographolide attenuates Gut-Brain-axis associated pathology in Gulf War Illness by modulating Bacteriome-Virome associated inflammation and microglia-neuron proinflammatory crosstalk. Brain Sciences. 11(7):905. https://doi.org/10.3390/brainsci11070905.
- Maqsood R, Reus JB, Wu LI, Holland LA, Nduati R, Mbori-Ngacha D, Maleche-Obimbo E, Begnel ER, Gantt S, Ojee E, Wamalwa D, John-Stewart G, Slyker J, Lehman DA, Lim ES. (2021) Breast milk virome and bacterial microbiome resilience in Kenyan women living with HIV. mSystems. 10.1128/mSystems.01079-20.
- Apakupakul K, Deem SL, Maqsood R, Sithiyopasakul P, Wang D, Lim ES. (2021) Endogenization of a prosimian retrovirus during lemur evolution. Viruses. 13(3):383. doi: 10.3390/v13030383.
- Ladner JT, Larsen BB, Bowers JR, Hepp CM, Bolyen E, Folkerts M, Sheridan K, Pfeiffer A, Yaglom H, Lemmer D, Sahl JW, Kaelin EA, Maqsood R, Bokulich NA, Quirk G, Watt TD, Komatsu K, Waddell V, Lim ES, Caporaso JG, Engelthaler DM, Worobey M, Keim P. (2020) An Early Pandemic Analysis of SARS-CoV-2 Population Structure and Dynamics in Arizona. mBio. 11(5):e02107-20.
Press release: Arizona genetic research group tracks initial spread of SARS-CoV-2. - Holland LA, Kaelin EA, Maqsood R, Estifanos B, Wu LI, Varsani A, Halden RU, Hogue BG, Scotch M, Lim ES. (2020) An 81 nucleotide deletion in SARS-CoV-2 ORF7a identified from sentinel surveillance in Arizona (Jan-Mar 2020). Journal of Virology. 94:e00711-20.
Press release: ASU scientific team finds new, unique mutation in coronavirus study. - Reus JB, Trivino-Soto GS, Wu LI, Kokott K, Lim ES. (2020) SV40 large T antigen is not responsible for the loss of STING in 293T cells but can inhibit cGAS-STING interferon induction. Viruses. 12, 137.
- Yaron JR, Ambadapadi S, Zhang L, Chavan RN, Tibbetts SA, Keinan S, Varsani A, Maldonado J, Kraberger S, Tafoya AM, Bullard WL, Kilbourne J, Stern-Harbutte A, Krajmalnik-Brown R, Munk BH, Koppang EO, Lim ES, Lucas AR. (2020) Immune protection is dependent on the gut microbiome in a lethal mouse gammaherpesviral infection. Scientific Reports. 10(1):2371.
- Maqsood R, Rodgers R, Rodriguez C, Handley SA, Ndao IM, Tarr PI, Warner BB, Lim ES, Holtz LR. (2019) Discordant transmission of bacteria and viruses from mothers to babies at birth. Microbiome. 7(1):156.
Press release: Mother-baby microbiome rush at birth can have lifelong health impact for the infant.
Video abstract: Bacteria and viruses are not inherited equally from mother to child at birth. - Seth RK, Maqsood R, Mondal A, Bose D, Kimono D, Holland LA, Lloyd PJ, Klimas N, Horner RD, Sullivan K, Lim ES, Chatterjee S. (2019) Gut DNA virome diversity and its association with host bacteria regulate inflammatory phenotype and neuronal immunotoxicity in experimental Gulf War illness. Viruses. 11(10).
Press release: Scientists find solution to Gulf War Illness in FDA-approved antiviral drugs. - Lim ES, Rodriguez C, Holtz LR. (2018) Amniotic fluid from healthy term pregnancies does not harbor a detectable microbial community. Microbiome. 6(1):87.
- Peretti A, Geoghegan EM, Pastrana DV, Smola S, Feld P, Sauter M, Lohse S, Ramesh M, Lim ES, Wang D, Borgogna C, FitzGerald PC, Bliskovsky V, Starrett GJ, Law EK, Harris RS, Killian JK, Zhu J, Pineda M, Meltzer PS, Boldorini R, Gariglio M, Buck CB. (2018) Characterization of BK polyomaviruses from kidney transplant recipients suggests a role for APOBEC3 in driving in-host virus evolution. Cell Host and Microbe. 23(5):628–635.
- Reddy KC, Dror T, Sowa JN, Panek J, Chen K, Lim ES, Wang D, Troemel ER. (2017) An Intracellular Pathogen Response Pathway Promotes Proteostasis in C. elegans. Current Biology. 27(22):3544-3553.
- Amatya R, Deem SL, Porton IJ, Wang D, Lim ES. Complete Genome Sequence of Torque teno indri virus 1, a Novel Anellovirus in Blood from a Free-Living Lemur. Genome Announcements. 2017 Jul 27;5(30). PMID: 28751399
- Baldauf HM, Stegmann L, Schwarz SM, Ambiel I, Trotard M, Martin M, Burggraf M, Lenzi GM, Lejk H, Pan X, Fregoso OI, Lim ES, Abraham L, Nguyen LA, Rutsch F, König R, Kim B, Emerman M, Fackler OT, Keppler OT. Vpx overcomes a SAMHD1-independent block to HIV reverse transcription that is specific to resting CD4 T cells. Proc Natl Acad Sci U S A. 2017 Mar 7;114(10):2729-2734. PMID: 28228523
- Janowski AB, Krishnamurthy SR, Lim ES, Zhao G, Brenchley JM, Barouch DH, Thakwalakwa C, Manary MJ, Holtz LR, Wang D. Statoviruses, A novel taxon of RNA viruses present in the gastrointestinal tracts of diverse mammals. Virology. 2017 Apr;504:36-44. PMID: 28152382
- Zhao G, Wu G, Lim ES, Droit L, Krishnamurthy S, Barouch DH, Virgin HW, Wang D. VirusSeeker, a computational pipeline for virus discovery and virome composition analysis. Virology. 2017 Mar;503:21-30. PMID: 28110145
- Lim ES, Brennan DC. A Snapshot of Antibody-Mediated Rejection Goes Viral. Transplantation. 2017 Feb;101(2):227. PMID: 27779575.
- Lim ES, Wang D, Holtz LR. The Bacterial Microbiome and Virome Milestones of Infant Development. Trends in Microbiology. 2016 Jun 25. PMID: 2735364
- Monaco CL, Gootenberg DB, Zhao G, Handley SA, Ghebremichael MS, Lim ES, Lankowski A, Baldridge MT, Wilen CB, Flagg M, Norman JM, Keller BC, Luévano JM, Wang D, Boum Y, Martin JN, Hunt PW, Bangsberg DR, Siedner MJ, Kwon DS, Virgin HW. Altered Virome and Bacterial Microbiome in Human Immunodeficiency Virus-Associated Acquired Immunodeficiency Syndrome. Cell Host and Microbe. 2016 Mar 9;19(3):311-322. doi: 10.1016/j.chom.2016.02.011. PMID: 26962942
- Lim ES, Zhou YJ, Zhao GY, Bauer I, Droit L, Ndao IM, Warner BB, Tarr PI, Wang D, Holtz LR. Early life dynamics of the human gut virome and bacterial microbiome in infants. Nature Medicine. 2015. Sep 14. doi: 10.1038/nm.3950. PMID: 26366711
*Highlighted in Nature Reviews Gastroenterology & Hepatology. Gut microbiota: The gut virome and bacterial microbiome-the early years. 2015 Sep 29. doi: 10.1038/nrgastro.2015.169.
*Evaluated on TWiV #355: Baby’s first virome. - Lim ES, Deem SL, Porton IJ, Cao S, Wang D. Species-specific transmission of novel picornaviruses in lemurs. Journal of Virology. 2015 Apr;89(7):4002-10. PMID: 25631076
- Lim ES, Meinerz NM, Primi B, Wang D, Garcea RL. Common exposure to STL polyomavirus during childhood. Emerging Infectious Diseases. 2014 Sep;20(9):1559-61. PMID: 25148144
- Lim ES, Cao S, Holtz LR, Antonio M, Stine OC, Wang D. Discovery of rosavirus 2, a novel variant of a rodent-associated picornavirus, in children from The Gambia. Virology. 2014 Apr;454-455:25-33. PMID: 24725928
- Lim ES, Reyes A, Antonio M, Saha D, Ikumapayi UN, Adeyemi M, Stine OC, Skelton R, Brennan DC, Mkakosya RS, Manary MJ, Gordon JI, Wang D. Discovery of STL polyomavirus, a polyomavirus of ancestral recombinant origin that encodes a unique T antigen by alternative splicing. Virology. 2013 Feb 20;436(2):295-303. PMID: 23276405
- Siebrasse EA, Reyes A, Lim ES, Zhao G, Mkakosya RS, Manary MJ, Gordon JI, Wang D. Identification of MW polyomavirus, a novel polyomavirus in human stool. Journal of Virology. 2012 Oct;86(19):10321-6. PMID: 22740408
- Lim ES, Wu LI, Malik HS, Emerman M. The function and evolution of the restriction factor Viperin in primates was not driven by lentiviruses. Retrovirology. 2012 Jun 26;9:55. PMID: 22734835
- Lim ES, Fregoso OI, McCoy CO, Matsen FA, Malik HS, Emerman M. The ability of primate lentiviruses to degrade the monocyte restriction factor SAMHD1 preceded the birth of the viral accessory protein Vpx. Cell Host and Microbe. 2012 Feb 16;11(2):194-204. PMID: 22284954
*Previewed by Planelles V. SAMHD1 Joins the red Queen's court. Cell Host and Microbe. 2012 Feb 16;11(2):103-5.
*Evaluated on Faculty of 1000. - Lim ES, Emerman M. HIV: Going for the watchman. Nature. 2011 Jun 29;474(7353):587-8. PMID: 21720361.
- Lim ES, Malik HS, Emerman M. Ancient adaptive evolution of tetherin shaped the functions of Vpu and Nef in human immunodeficiency virus and primate lentiviruses. Journal of Virology. 2010 Jul;84(14):7124-34. PMID: 20444900
- Spindler KR, Welton AR, Lim ES, Duvvuru S, Althaus IW, Imperiale JE, Daoud AI, Chesler EJ. The major locus for mouse adenovirus susceptibility maps to genes of the hematopoietic cell surface-expressed LY6 family. Journal of Immunology. 2010 Mar 15;184(6):3055-62. PMID: 20164425
- Lim ES, Emerman M. Simian immunodeficiency virus SIVagm from African green monkeys does not antagonize endogenous levels of African green monkey tetherin/BST-2. Journal of Virology. 2009 Nov;83(22):11673-81. PMID: 19726508
Research Activity
Lim Lab in the News
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January 29, 2021. First Cases of UK COVID-19 Variant Detected in Arizona. Arizona Department of Health Services.
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September 15, 2020. Arizona genetic research group tracks initial spread of SARS-CoV-2. ASU News.
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May 5, 2020. ASU scientific team finds new, unique mutation in coronavirus study. ASU News.
Also featured in ASU Now’s year in review top stories from 2020. -
January 30, 2020. Mother-baby microbiome rush at birth can have lifelong health impact for the infant. ASU News.
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October 24, 2019. Scientists find solution to Gulf War illness in FDA-approved antiviral drugs. ASU News.
Teaching Website
Courses
| Summer 2021 | |
|---|---|
| Course Number | Course Title |
| MIC 495 | Undergraduate Research |
| Spring 2021 | |
|---|---|
| Course Number | Course Title |
| BIO 493 | Honors Thesis |
| MIC 494 | Special Topics |
| BIO 494 | Special Topics |
| MIC 495 | Undergraduate Research |
| BIO 495 | Undergraduate Research |
| Fall 2020 | |
|---|---|
| Course Number | Course Title |
| MIC 220 | Biology of Microorganisms |
| BIO 493 | Honors Thesis |
| MIC 495 | Undergraduate Research |
| BIO 495 | Undergraduate Research |
| Summer 2020 | |
|---|---|
| Course Number | Course Title |
| MIC 495 | Undergraduate Research |
| Spring 2020 | |
|---|---|
| Course Number | Course Title |
| MIC 492 | Honors Directed Study |
| BIO 495 | Undergraduate Research |
| Fall 2019 | |
|---|---|
| Course Number | Course Title |
| MIC 220 | Biology of Microorganisms |
| BIO 495 | Undergraduate Research |
| Summer 2019 | |
|---|---|
| Course Number | Course Title |
| MIC 495 | Undergraduate Research |
| Spring 2019 | |
|---|---|
| Course Number | Course Title |
| MIC 494 | Special Topics |
| BIO 494 | Special Topics |
| Fall 2018 | |
|---|---|
| Course Number | Course Title |
| MIC 220 | Biology of Microorganisms |
| Spring 2018 | |
|---|---|
| Course Number | Course Title |
| MIC 494 | Special Topics |
| BIO 494 | Special Topics |
Presentations
MIC 494/BIO 494 - Human Pathogenic Viruses and Infectious Diseases (3.0 credits)
Class is offered in the Spring semesters.
Tues, Thur. 3:00 pm - 4:15 pm.
Location to be determined (Tempe campus).
Course description: Students will learn basic and advanced concepts in medical virology. The major emphasis will be on significant human diseases caused by viral pathogens including SARS-CoV-2, HIV, ebola, influenza, measles and others.
MIC 220 - Biology of Microorganisms (3.0 credits)
Class is offered in Fall and Spring semesters (I teach the Fall courses)
Mon, Wed. 12:00 pm - 1:15 pm.
Location to be deteremined (Tempe campus).
Course description: Introductory microbiology for students majoring in the life sciences. Detailed study of microbial cells, their structure, genetics, physiology and taxonomy.
Course schedule and other information:
https://viromelab.org/courses/
Honors/Awards
2016 NIH Pathway to Independence Award (K99/R00), National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK)
2013 - 2016 The Eli & Edythe Broad Fellowship, Life Sciences Research Foundation
2011 - 2012 Helen Riaboff Whiteley Graduate Fellowship Award, University of Washington, Dept. of Microbiology
2009 - 2011 Fred Hutchinson Cancer Research Center Interdisciplinary Training Fellowship
2010 Young Investigator Award. 17th Conference on Retroviruses and Opportunistic Infections (CROI)
2009 Neal B. Groman Teaching Award, University of Washington Dept. of Microbiology, Seattle, WA
Editorships
Academic Editor, PLOS ONE
Topic Editorial Board, Viruses
Young Investigator Editorial Board, AIDS Research and Human Retroviruses
Professional Associations
American Society for Virology, Program Planning Committee
Service
Division Lead, Arizona Wellbeing Commons - Viruses, Immunity, Microbiomes and Infectious Diseases
Novel coronavirus information
Spring 2021 update | FAQ page | Class flexibility for students | Novel coronavirus updates