Spencer Nyholm

Professor

Molecular and Cell Biology / Microbiology

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Education: Ph.D. University of Hawaii; Postdoctoral studies, Stanford University/Harvard University

Research Interests: Symbiosis; comparative immunology

The goal of my laboratory is to understand the mechanisms by which animal hosts and microbial symbionts communicate with an emphasis on how components of the innate immune system may influence these interactions.

We use the symbiosis between the Hawaiian bobtail squid, Euprymna scolopes, and the bioluminescent bacterium, Vibrio fischeri, as a model system to study the effects of beneficial bacteria on animal host tissues. This association has an advantage in that each partner can be raised independently in the laboratory and is readily available for molecular, biochemical, and genetic analyses.

My lab also is engaged in a project using functional genomics to study the relationship between hydrothermal vent tubeworms and their chemoautotrophic, sulfide-oxidizing bacterial symbionts.

Selected Publications:

Lisa Rouressol, John Briseno, Nidhi Vijayan, Grischa Y. Chen, Elena A. Ritschard, Gustavo Sanchez, Spencer V. Nyholm, Margaret J. McFall-Ngai, Oleg Simakov, Emergence of novel genomic regulatory regions associated with light-organ development in the bobtail squid, iScience, Volume 26, Issue 7, 2023, 107091, ISSN 2589-0042, https://doi.org/10.1016/j.isci.2023.107091.

McAnulty SJ, Kerwin AH, Koch E, Nuttall B, Suria AM, Collins AJ, Schleicher TR, Rader BA, Nyholm SV. “Failure To Launch”: Development of a Reproductive Organ Linked to Symbiotic Bacteria. mBio. 2023 Jan 19:e0213122. doi: 10.1128/mbio.02131-22. Epub ahead of print. PMID: 36656023

Allison H. Kerwin, Sarah J. McAnulty, and Spencer V. Nyholm Development of the Accessory Nidamental Gland and Associated Bacterial Community in the Hawaiian Bobtail Squid, Euprymna scolopes. The Biological Bulletin Volume 240, Number 3, 2021, https://www.journals.uchicago.edu/doi/pdf/10.1086/713965

Nyholm, S.V., McFall-Ngai, M.J. A lasting symbiosis: how the Hawaiian bobtail squid finds and keeps its bioluminescent bacterial partner. Nat Rev Microbiol 19, 666–679 (2021). https://doi.org/10.1038/s41579-021-00567-y

Kerwin AH*, Gromek SM*, Suria AM, Samples RM, Deoss DJ, O’Donnell K, Frasca Jr. S, Sutton DA, Wiederhold NP, Balunas MJ^#, Nyholm SV^# (2019) Shielding the next generation: symbiotic bacteria from a reproductive organ protect bobtail squid eggs from fungal fouling. mBio 10(5). pii: e02376-19. doi: 10.1128/mBio.02376-19. (*contributed equally; ^#corresponding)

Baker LJ, Freed LL, Easson CG, Lopez JV, Fenolio D, Sutton TT, Nyholm SV, Hendry TA (2019) Diverse deep-sea anglerfishes share a genetically reduced luminous symbiont that is acquired from the environment. Elife Oct 1;8. pii: e47606. doi: 10.7554/eLife.47606

Lynch JB, Schwartzman JA, Bennett BD, McAnulty SJ, Knop M, Nyholm SV, Ruby EG (2019) Ambient pH alters the protein content of outer membrane vesicles, driving host development in a beneficial symbiosis. J. Bacteriol. 201 (20) pii:e00319-19. doi: 10.1128/JB.00319-19 

Rader BA, McAnulty SJ, Nyholm SV (2019) Persistent symbiont colonization leads to a maturation of hemocyte response in the Euprymna scolopes/Vibrio fischeri symbiosis. Microbiology Open Jun 13:e858. doi: 10.1002/mbo3.858 

Kerwin AH, Nyholm SV (2018) Reproductive system symbiotic bacteria are conserved between two distinct populations of Euprymna scolopes from Oahu, HI. mSpheredoi: 10.1128/mSphere.00531-17. eCollection 2018 Mar-Apr. PMID: 29600280 (cover image March/April 2018)

Kerwin AH, Nyholm SV. (2017) Symbiotic bacteria associated with a bobtail squid reproductive system are detectable in the environment, and stable in the host and developing eggs. Environ Microbiol. doi: 10.1111/1462-2920.13665.

McAnulty SJ, Nyholm SV. (2017) The Role of Hemocytes in the Hawaiian Bobtail Squid, Euprymna scolopes: A Model Organism for Studying Beneficial Host-Microbe Interactions. Front Microbiol. doi: 10.3389/fmicb.2016.02013.

Gromek SM, Suria AM, Fullmer MS, Garcia JL, Gogarten JP, Nyholm SV and Balunas MJ (2016) Leisingera sp. JC1, a Bacterial Isolate from Hawaiian Bobtail Squid Eggs, Produces Indigoidine and Differentially Inhibits Vibrios. Front. Microbiol. 7:1342. doi: 10.3389/fmicb.2016.01342.

Collins AJ, Fullmer MS, Gogarten JP, Nyholm SV (2015). Comparative genomics of Roseobacter clade bacteria isolated from the accessory nidamental gland of Euprymna scolopes. Front Microbiol. 2015 Feb 23;6:123. doi: 10.3389/fmicb.2015.00123. eCollection 2015. PMID:  25755651  [PubMed]

Schleicher TR, VerBerkmoes NC, Shah M, Nyholm SV. (2014). Colonization state influences the hemocyte proteome in a beneficial squid-vibrio symbiosis. Mol Cell Proteomics. 2014 Jul 18. pii: mcp.M113.037259. [Epub ahead of print]

Schleicher TR, Nyholm SV (2011) Characterizing the host and symbiont proteomes between the bobtail squid, Euprymna scolopes, and the bacterium, Vibrio fischeri. PLoS One. 6(10):e25649

Collins AJ, Nyholm SV (2011) Draft genome of Phaeobacter gallaeciensis ANG1; a dominant member of the accessory nidamental gland of Euprymna scolopes. J. Bacteriol. 193: 3397-3398.

Collins AJ, Nyholm SV (2010) Obtaining Hemocytes from the Hawaiian Bobtail Squid Euprymna scolopes and Observing their Adherence to Symbiotic and Non-Symbiotic Bacteria. JoVE. 36. http://www.jove.com/index/details.stp?id=1714, doi: 10.3791/1714

Wier AM, Nyholm SV, Mandel MJ, Massengo-Tiassé RP, Schaefer AL, Koroleva I, Splinter-Bondurant S, Brown B, Manzella L, Snir E, Almabrazi H, Scheetz TE, Bonaldo Mde F, Casavant TL, Soares MB, Cronan JE, Reed JL, Ruby EG, McFall-Ngai MJ. (2010) Transcriptional patterns in both host and bacterium underlie a daily rhythm of anatomical and metabolic change in a beneficial symbiosis. Proc. Nat. Acad. Sci., USA, 107, 2259-64

McFall-Ngai MJ, Nyholm SV, Castillo MG (2009) The role of the immune system in the initiation and persistence of the Euprymna scolopes-Vibrio fischeri symbiosis. Semin. Immunol. 22: 48-53.

Nyholm SV, Stewart JJ, Ruby EG, McFall-Ngai MJ (2009) Recognition between symbiotic Vibrio fischeri and the haemocytes of Euprymna scolopes. Environ. Microbiol. 11: 483-93.

Nyholm, SV (2009) Peptidoglycan monomer release and Vibrio fischeri. J. Bacteriol. 191:1997-1999.

Nyholm SV, Nishiguchi MK (2008) The evolutionary ecology of a sepiolid squid-Vibrio association: from cell to environment. Vie et Milieu 58: 175-184.

Spencer V. Nyholm, Julie Robidart and Peter R. Girguis. 2008. Coupling metabolite flux to transcriptomics: insights into the molecular mechanisms underlying primary productivity by the hydrothermal vent tubeworm Ridgeia piscesae. Biol. Bull. 214: 255-265.
Symbiosis

Nyholm, S.V. and M. J. McFall-Ngai. 2004. The Winnowing: Establishing the Squid-Vibrio Symbiosis. Nature Rev. Microbiol. 2: 632-642.

Nyholm, S. V. and M. J. McFall-Ngai. 2003. Dominance of Vibrio fischeri in secreted mucus outside the light organ of Euprymna scolopes: the first site of symbiont specificity. Appl. Environ. Microbiol. 69: 3932-7.

Nyholm, S. V., B. Deplancke, H. R. Gaskins, M. A. Apicella, and M. J. McFall-Ngai. 2002. Roles of nonsymbiotic and symbiotic bacteria in the dynamics of mucus secretion during symbiont colonization of the Euprymna scolopes light organ. Appl. Environ. Microbiol. 68:5113-5122.

Nyholm, S. V., E. V. Stabb, E. G. Ruby, and M. J. McFall-Ngai. 2000 Establishment of an animal-bacterial association: recruiting symbiotic vibrios from the environment. Proc. Nat. Acad. Sci., USA 97:10231-10235.

Nyholm, S. V. and M. J. McFall-Ngai. 1998. Sampling the light-organ microenvironment of Euprymna scolopes: description of a population of host cells in association with the bacterial symbiont Vibrio fischeri. Biol. Bull. 195: 89-97.

Other publications:

Nyholm, S.V., Passegue, E., Ludington, W.B., Voskoboynik, A., Mitchel, K., Weissman, I.L., DeTomaso, A. W. (2006) Fester, a candidate allorecognition receptor from a primitive chordate. Immunity. 25: 163-73.

De Tomaso, A.W., Nyholm, S.V., Palmeri, K.J., Ishizuka, K.J., Ludington, W.B., Mitchel, K., Weissman, I.L. 2005. Isolation and characterization of a protochordate histocompatibility locus. Nature. 438:454-9.