Microbiology Program

Publications

Check out the recent publications from participating NASA scientists, Principal Investigators, and contributors from universities and labs around the world:

Pedro Madrigal, Nitin K. Singh, Jason M. Wood, Elena Gaudioso, Félix Hernández-del-Olmo, Christopher E. Mason, Kasthuri Venkateswaran, Afshin Beheshti, Machine learning algorithm to characterize antimicrobial resistance associated with the International Space Station surface microbiome, bioRxiv 2022.02.07.479455; doi: https://doi.org/10.1101/2022.02.07.479455

An, R., & Lee, J. A. (2022). CAMDLES: CFD-DEM Simulation of Microbial Communities in Spaceflight and Artificial Microgravity. Life, 12(5), 660.

Lombardino, J., Bijlani, S., Singh, N. K., Wood, J. M., Barker, R., Gilroy, S., . . . Venkateswaran, K. (2022). Genomic Characterization of Potential Plant Growth-Promoting Features of Sphingomonas Strains Isolated from the International Space Station. Microbiology Spectrum, 10(1), e01994-01921.

Madrigal P, Singh NK, Wood JM, Gaudioso E, Hernández-del-Olmo F, Mason CE, Venkateswaran K, Beheshti A. Machine learning algorithm to characterize antimicrobial resistance associated with the International Space Station surface microbiome. bioRxiv 2022.02.07.479455.

Singh, N. K., Lavire, C., Nesme, J., Vial, L., Nesme, X., Mason, C. E., . . . Venkateswaran, K. (2022). Comparative Genomics of Novel Agrobacterium G3 Strains Isolated From the International Space Station and Description of Agrobacterium tomkonis sp. nov. Frontiers in Microbiology, 3369.

Tesei, D., Jewczynko, A., Lynch, A. M., & Urbaniak, C. (2022). Understanding the Complexities and Changes of the Astronaut Microbiome for Successful Long-Duration Space Missions. Life, 12(4), 495.

Contributions of spore secondary metabolites to UV-C protection and virulence vary in different Aspergillus fumigatus strains. Blachowicz A, Raffa N, Bok JW, Choera T, Knox B, Lim FY, Huttenlocher A, Wang CCC, Venkateswaran K, Keller NP. MBio. 2020 Feb 18;11(1):e03415-19.

This study exposed various A. fumigatus mutants to UV-C radiation to understand the role of secondary metabolites show differential roles of secondary metabolites in spore protection and found it’s dependent on the environmental stress and strain of A. fumigatus

Genomic and phenotypic characterization of Burkholderia isolates from the potable water system of the International Space Station. O'Rourke A, Lee MD, Nierman WC, Everroad RC, Dupont CL. PLoS One. 2020 Feb 20;15(2):e0227152.

This study studied two ISS isolates from the water supply - Burkholderia cepacia and Burkholderia contaminans - found that while the populations of Burkholderia present in the ISS PWS each maintain virulence, they are likely are not more virulent than those that might be encountered on planet and remain susceptible to clinically used antibiotics.

The EcAMSat fluidic system to study antibiotic resistance in low Earth orbit: Development and lessons learned from space flight. Padgen MR, Chinn TN, Friedericks CR, Lera MP, Chin M, Parra MP, Piccini ME, Ricco AJ, Spremo SM. Acta Astronaut. 2020 Feb 19. [Article in Press]

Results showed that the ΔrpoS mutant of E.coli was 34-37% less metabolically active than the WT for four different sets of conditions: ground without Gm, ground with Gm; μ-g without Gm, μ-g with Gm. These findings indicate that the rpoS gene and its downstream products are important therapeutic targets for treating bacterial infections in space, much as they are on the ground.

In situ linkage of fungal and bacterial proliferation to microbiologically influenced corrosion in B20 biodiesel storage tanks. Stamps BW, Bojanowski CL, Drake CA, Nunn HS, Lloyd PF, Floyd JG, Emmerich KA, Neal AR, Crookes-Goodson WJ, Stevenson BS.

Front Microbiol. 2020 Feb 25;11:167. (Stamps, Sloan/MoBE NPP)

This is the first in situ study of this scale incorporating community and corrosion measurements in an active biodiesel storage environment. A filamentous fungus within the family Trichocomaceae, not yet widely recognized as a contaminant of petroleum fuels was found to be significantly correlated with visible fouling and pitting corrosion.

Identification of metagenome-assembled genomes containing antimicrobial resistance genes, isolated from an advanced water treatment facility. Stamps BW, Spear JR. Microbiol Resour Announc. 2020 Apr 2;9(14):e00003-20. (Stamps, Sloan/MoBE NPP)

This study isolated 95 metagenome-assembled genomes (MAGs) that harbor antimicrobial resistance genes from samples obtained in a large advanced wastewater reclamation facility prior to microfiltration.

The influence of spaceflight on the astronaut salivary microbiome and the search for a microbiome biomarker for viral reactivation. Urbaniak C, Lorenzi H, Thissen J, Jaing C. Crucian B, Sams C, Pierson D, Venkateswaran K, Mehta S. Microbiome 8, 56 (2020).
(Jaing, 80NSSC18K0113. Venkat, 19-12829-26, Urbaniak, SB NPP Felllow)

Salivary microbiome from 10 astronauts was analyzed for Epstein-Barr virus (EBV), herpes simplex virus (HSV), and varicella zoster virus (VZV) pre-flight, in-flight, and post-flight. Streptococcus was the most abundant organism in the saliva, making up 8% of the total organisms detected, and their diversity decreased during spaceflight.

Crewmember microbiome may influence microbial composition of ISS habitable surfaces. Avila-Herrera, A., Thissen, J., Urbaniak, C., Be, N. A., Smith, D. J., Karouia, F., ... & Jaing, C. (2020). PloS one, 15(4), e0231838. (Jaing, 80NSSC18K0113, Venkat, 47-700062, Mehta, 80NSSC18K0113, Smith)

Of the eight crew body sites that were analyzed, those of skin, nostril, and ear samples were found to be more similar to the microbe populations found on ISS surfaces than mouth and saliva samples; and that the microbial composition of the crew skin samples were more closely related to the ISS surface samples collected by the crewmember on the same flight than ISS surface samples collected by other crewmembers on different flights. One study has, for the first time, examined correlations between resident astronauts and the ISS surface microbiomes and found that surface microbiome shares similarities to the skin microbiome.

Characterization of the total and viable bacterial and fungal communities associated with the International Space Station surfaces. Sielaff AC, Urbaniak C, Malli Mohan GB, Stepanov VG, Tran Q, Wood JM, Minich J, McDonald D, Mayer T, Knight R, Karouia F, Fox GE and Venkateswaran K. Microbiome, April, 2019 7:50. (Venkat, 19-12829-26)

This study used molecular and culture-based methods to assess microbial communities on ISS 8 different surfaces spanning 14 months and analyzed upon return to Earth. This study provides the first comprehensive catalog of both total and intact/viable bacteria and fungi found on surfaces in closed space systems and can be used to help develop safety measures that meet NASA requirements for deep space human habitat.

The risk of Staphylococcus skin infection during space travel and mitigation strategies.Xiao S, Venkateswaran KJ, Jiang SC. Microbial Risk Analysis. 2018 Aug 16. (Venkat, 19-12829-26)

The research objective of this study was to develop a quantitative microbial risk assessment (QMRA) for modeling the risk of S. aureus skin infections in astronauts. Prevention and control of bacterial skin infections by once daily and twice daily cleanings resulted in 84.2% and 96.1% reductions, respectively. The comparative risk analysis as used in this study offers a scientific basis regarding the effectiveness of interventions (skin cleaning regimens) in mitigating skin infection risks during spaceflight.

Genomic Characterization and Virulence Potential of Two Fusarium oxysporum Isolates Cultured from the International Space Station. Urbaniak C, van Dam P, Zaborin A, Zaborina O, Gilbert JA, Torok T, Wang C, Venkateswaran K. mSystems Mar 2019, 4 (2). (Venkat, 19-12829-26 and Urbaniak, NPP)

Two isolates of Fusarium oxysporum, ISS-F3 and ISS-F4, were cultured from the dining table on the International Space Station (ISS). F. oxysporum strains are well known for their plant pathogenicity. While genomic analysis showed that these ISS strains are unlikely to be plant pathogens, a virulence assay using an immunocompromised Caenorhabditis elegans model of fusariosis revealed that they were virulent and may represent opportunistic pathogens in animals, including humans.

Metagenome to phenome approach enables isolation and genomics characterization of Kalamiella piersonii gen. nov., sp. from the International Space Station. Singh NK, Wood JM, Mhatre SS, Venkateswaran K. Applied Microbiology and Biotechnology 2019. (Venkat, NNH12ZTT001N & post-doctoral fellowships for NKS, JMW and SSM.)

Several evolutionarily distinct, near full-length draft metagenome-resolved genomes (MRG), were assembled from sequences recovered from the International Space Station (ISS) environments. This approach to isolating microbes allowed for the characterization of functional pathways and their potential virulence properties that can directly affect human health.

Recent advances in the genome mining of Aspergillus secondary metabolites (covering 2012–2018). Romsdahl J, Wang CC. MedChemComm. 2019. Review. (Wang, NNX15AB49G)

This review covers advances made in genome mining SMs produced by Aspergillus nidulans, Aspergillus fumigatus, Aspergillus niger, and Aspergillus terreus in the past six years (2012–2018). Genetic identification and molecular characterization of SM biosynthetic gene clusters, along with proposed biosynthetic pathways, are discussed.

Yeast in Space. Hammond T.G., Birdsall H.H.

In: Pathak Y., Araújo dos Santos M., Zea L. (eds) Handbook of Space Pharmaceuticals. Springer, Cham 2019. (Hammond, NNX12AM93G)

This review describes previous work that has been done using a library of gene-deletion species of S. cerevisiae to characterize the genes involved in the response to spaceflight. This book chapter reviews the ways that yeast can be used to develop and test countermeasures. Broad stimulus libraries of gene-deleted yeast, including radiation types and radiomimetics, have been collected and assessed at 20+ generations are available for comparison.

Vaccines in Space. Hammond T.G., Birdsall H.H.

In: Pathak Y., Araújo dos Santos M., Zea L. (eds) Handbook of Space Pharmaceuticals. Springer, Cham 2019. (Hammond, NNX12AM93G)

Review of the findings of microbial virulence across multiple species and on the ground and spaceflight conditions. Authors recommend the use of the nematode, C. elegans, as an infection model to study host-pathogen interactions for potentially harmful microbes.

Proteomic and Metabolomic Characteristics of Extremophilic Fungi Under Simulated Mars Conditions. Blachowicz A, Chiang AJ, Elsaesser A, Kalkum M, Ehrenfreund P, Stajich JE, Torok T, Wang CC, Venkateswaran K. Frontiers in Microbiology. 2019;10:1013. (Venkat, Microbial Observatory funding acknowledged)

This study is the first report of fungal survival after exposure of monolayers of conidia (spores) to simulated Mars conditions. Surviving strains were further characterized for proteomic, and metabolomic changes. Differential expression of proteins involved in ribosome biogenesis, translation, and carbohydrate metabolic processes was observed. Lastly, the fungal spores that were re-exposed to UV-C exhibited enhanced resistance when compared to the unexposed strains.

Cellular Responses And Gene Expression Profile Changes Due To Bleomycin-Induced DNA Damage In Human Fibroblasts In Space.
PLOS ONE. 2017 March 1; 12(3): e0170358.
Lu, T., Zhang, Y., Kidane, Y., Feiveson, A.H., Stodieck, L.S., Karouia, F., Ramesh, G.T., Rohde, L., Wu, H.
DOI: 10.1371/journal.pone.0170358.

Detection Of DNA Damage By Space Radiation In Human Fibroblasts Flown On The International Space Station.
Lu, T., Zhang, Y., Wong, M., Feiveson, A.H., Gaza, R., Stoffle, N.N., Wang, H., Wilson, B., Rohde, L., Stodieck, L.S., Karouia,
F., Wu, H.
Life Sciences in Space Research. 2017 February; 12: 24-31.
DOI: 10.1016/j.lssr.2016.12.004.

Transient Gene And MicroRNA Expression Profile Changes Of Confluent Human Fibroblast Cells In Spaceflight.
Zhang, Y., Lu, T., Wong, M., Wang, X., Stodieck, L.S., Karouia, F., Story, M., Wu, H.
FASEB: Federation of American Societies for Experimental Biology Journal. 2016 February 25; epub: fj.201500121.
DOI: 10.1096/fj.201500121. PMID: 26917741.

Cellular Response of Escherichia coli to Microgravity and Microgravity Analogue Culture.
Singh, R., & Matin, A. Effect of Spaceflight and Spaceflight Analogue Culture on Human and Microbial Cells (2016). (pp. 259-282): Springer.

Draft Genome Sequences of Two Aspergillus fumigatus Strains, Isolated from the International Space Station.
Singh, N. K., Blachowicz, A., Checinska, A., Wang, C., & Venkateswaran, K. (2016). Genome Announc, 4(4). DOI:10.1128/genomeA.00553-16.

Effects of Microgravity and Clinorotation on the Virulence of Klebsiella, Streptococcus, Proteus, and Pseudomonas.
Hammond, T. G., Stodieck, L., Birdsall, H. H., Koenig, P., Hammond, J. S., Gunter, M., & Allen, P. L. (2016). Gravitational and Space Research, 4(1).

A novel blue-light phototropic response is revealed in roots of Arabidopsis thaliana in microgravity.
Vandenbrink, J. P., Herranz, R., Medina, F. J., Edelmann, R. E., & Kiss, J. Z. (2016). Planta. DOI:10.1007/s00425-016-2581-8.

Microbiomes of the dust particles collected from the International Space Station and Spacecraft Assembly Facilities.
Checinska, A., Probst, A. J., Vaishampayan, P., White, J. R., Kumar, D., Stepanov, V. G., . . . Venkateswaran, K. (2015). Microbiome, 3(1), 50. DOI:10.1186/s40168-015-0116-3.

Genes Required For Survival In Microgravity Revealed By Genome-Wide Yeast Deletion Collections Cultured During Spaceflight.
Nislow, C., Lee, A.Y., Allen, P.L., Giaever, G., Smith, A., Gebbia, M., Stodieck, L.S., Hammond, J.S., Birdsall, H.H., Hammond, T.G.
BioMed Research International. 2015; 2015(976458): 10 pp.
DOI: 10.1155/2015/976458.

Light and gravity signals synergize in modulating plant development.
Vandenbrink, J. P., Kiss, J. Z., Herranz, R., & Medina, F. J. (2014). Front Plant Sci, 5, 563. DOI:10.3389/fpls.2014.00563.

Effect Of Spaceflight On Pseudomonas Aeruginosa Final Cell Density Is Modulated By Nutrient And Oxygen Availability.
Kim, W., Tengra, F.K., Shong, J., Marchand, N., Chan, H.K., Young, Z., Pangule, R.C., Parra, M.P., Dordick, J.S., Plawsky, J.L., Collins, C.H.
BMC Microbiology. 2013 November 6; 13(1): 241.
DOI: 10.1186/1471-2180-13-241. PMID: 24192060.

Spaceflight Promotes Biofilm Formation by Pseudomonas aeruginosa.
Kim, W., Tengra, F.K., Shong, J., Marchand, N., Chan, H.K., Young, Z., Pangule, R.C., Parra, M.P., Dordick, J.S., Plawsky, J.L., Collins, C.H.
PLOS ONE. 2013 April 29; 8(4): e62437.
DOI: 10.1371/journal.pone.0062437.

Effects of microgravity on the virulence of Listeria monocytogenes, Enterococcus faecalis, Candida albicans, and methicillin-resistant Staphylococcus aureus.
Hammond, T. G., Stodieck, L., Birdsall, H. H., Becker, J. L., Koenig, P., Hammond, J. S., . . . Allen, P. L. (2013). Astrobiology, 13(11), 1081-1090. DOI:10.1089/ast.2013.0986

Spaceflight Enhances Cell Aggregation And Random Budding In Candida Albicans.
Crabbe A., Nielson-Preiss S., Woolley C. M., Barrila J., Buchanan K., McCracken J., Inglis D. O., Searles S. C., Nelman-Gonzalez M. A., Ott C. M., Wilson J. W., Pierson D. L., Stefanyshyn-Piper H. M., Hyman L. E., Nickerson C. A.
PLOS ONE. 2013 December 4; 8(12): e80677.
DOI: 10.1371/journal.pone.0080677.

Effects of microgravity on the virulence of Salmonella toward Caenorhabditis elegans.
Hammond, T. G., Stodieck, L., Birdsall, H. H., Becker, J., Koenig, P., Hammond, J. S., . . . Allen, P. L. (2013). New Space, 1(3), 123-131.

Transcriptional and proteomic responses of Pseudomonas aeruginosa PAO1 to spaceflight conditions involve Hfq regulation and reveal a role for oxygen.
Crabbe, A., Schurr, M. J., Monsieurs, P., Morici, L., Schurr, J., Wilson, J. W., . . . Nickerson, C. A. (2011). Appl Environ Microbiol, 77(4), 1221-1230. DOI:10.1128/aem.01582-10.

Modeled microgravity increases filamentation, biofilm formation, phenotypic switching, and antimicrobial resistance in Candida albicans.
Searles, S. C., Woolley, C. M., Petersen, R. A., Hyman, L. E., & Nielsen-Preiss, S. M. (2011). Astrobiology, 11(8), 825-836. DOI:10.1089/ast.2011.0664.

Effect of spaceflight on Pseudomonas aeruginosa final cell density is modulated by nutrient and oxygen availability.
Kim, W., Tengra, F.K., Shong, J., Marchand, N., Chan, H.K., Young, Z., Pangule, R.C., Parra, M.P., Dordick, J.S., Plawsky, J.L., Collins, C.H.
BMC Microbiology. 2013 November 6; 13(1): 241.
DOI: 10.1186/1471-2180-13-241. PMID: 24192060.

Transcriptional And Proteomic Responses Of Pseudomonas Aeruginosa PAO1 To Spaceflight Conditions Involve Hfq Regulation And Reveal A Role For Oxygen.
Crabbe A, Schurr MJ, Monsieurs P, Morici L, Schurr J, Wilson JW, Ott CM, Tsaprailis G, Pierson DL, Stefanyshyn-Piper HM, Nickerson CA.
Applied and Environmental Microbiology. 2011; 77(4): 1221-1230. DOI: 10.1128/AEM.01582-10.
PMID: 21169425.

Response of Pseudomonas aeruginosa PAO1 to low shear modelled microgravity involves AlgU regulation.
Crabbé, A., Pycke, B., Van Houdt, R., Monsieurs, P., Nickerson, C., Leys, N., & Cornelis, P. (2010). Environmental microbiology, 12(6), 1545-1564.

Space Flight Alters Bacterial Gene Expression And Virulence And Reveals A Role For Global Regulator Hfq.
Wilson J. W., Ott C. M., Honer zu Bentrup K., Ramamurthy R., Quick L., Porwollik S., Cheng P., McClelland M., Tsaprailis G., Radabaugh T., Hunt A., Fernandez D., Richter E., Shah M., Kilcoyne M., Joshi L., Nelman-Gonzalez M. A., Hing S. M., Parra M. P., Dumars P. M., Norwood K. L., Devich J., Bober R., Ruggles A. D., Goulart C., Rupert M., Stodieck L. S., Stafford P., Catella L. A., Schurr M. J., Buchanan K., Morici L., McCracken J., Allen P. L., Baker-Coleman C., Hammond T. G., Vogel J., Nelson R., Pierson D. L., Stefanyshyn-Piper H. M., Nickerson C. A.
Proceedings of the National Academy of Sciences of the United States of America.
2007; 104(41): 16299-16304. DOI: 10.1073/pnas.0707155104.
PMID: 17901201.

The RNA Chaperone Hfq Is Essential For The Virulence Of Salmonella Typhimurium.
Sittka, A., Pfeiffer, V., Tedin, K., Vogel, J.
Molecular Microbiology. 2007; 63(1): 193-217. DOI: 10.1111/j.1365-2958.2006.05489.x
PMID: 17163975.

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