{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,30]],"date-time":"2026-07-30T09:19:19Z","timestamp":1785403159743,"version":"3.56.0"},"reference-count":39,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2026,5,20]],"date-time":"2026-05-20T00:00:00Z","timestamp":1779235200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Jet Propulsion Laboratory, California Institute of Technology","award":["JPL-1694993"],"award-info":[{"award-number":["JPL-1694993"]}]},{"award":["JPL-1694993"],"award-info":[{"award-number":["JPL-1694993"]}],"id":[{"id":"https:\/\/ror.org\/027k65916","id-type":"ROR","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000104","name":"National Aeronautics and Space Administration","doi-asserted-by":"crossref","award":["80NM0018D0004"],"award-info":[{"award-number":["80NM0018D0004"]}],"id":[{"id":"10.13039\/100000104","id-type":"DOI","asserted-by":"crossref"}]},{"award":["80NM0018D0004"],"award-info":[{"award-number":["80NM0018D0004"]}],"id":[{"id":"https:\/\/ror.org\/027ka1x80","id-type":"ROR","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Mars Sample Return Program planning includes a series of spacecraft staged both on the Martian surface and in low-Mars-orbit (LMO). During the transfer of samples into orbit, external spacecraft surfaces might be exposed to Mars dust carried on the sample container exterior and possibly extant microbiota (if present). This study was designed to characterize the synergistic effects of LMO ultraviolet irradiation, vacuum, and solar heating on the survival of two UV-resistant and heat-tolerant bacteria, one yeast, and one fungus. The species tested were Bacillus pumilus SAFR-032 spores, Geobacillus stearothermophilus ATCC 12980 spores, Naganishia onofrii DBVPG 5303 cells, and Aspergillus fumigatus ISSFT-021-30 spores, respectively. Spores of A. fumigatus ISSFT-021-30 and B. pumilus were also exposed to LMO conditions with and without a Mojave Mars Simulant (MMS) dust layer. Based on the data, the time required to reach the desired Sterility Assurance Level (SAL; dose-defined to yield a \u221212 log reduction) was 2.0 h for A. fumigatus ISSFT-021-30 and 76.6 min for B. pumilus SAFR-032 if exposed directly to the solar UV beam under LMO conditions. With the MMS present, predicted times to reach one SAL were extended to 22 h and 1.72 h, respectively. Analysis of UV transmittance through cell stacks of up to 12 \u00b5m thick was performed for A. fumigatus ISSFT-021-30. Results indicated that ~4\u20135% of UVC photons can penetrate through 12 \u00b5m stacked aggregates of spores. These findings indicate that (1) the LMO environment can be used to attain the mandated levels of spacecraft surface bioburden reductions and (2) dust shielding and microbial aggregation attenuate UV irradiation, leading to extended orbital residence times to achieve mandated bioburden reductions.<\/jats:p>","DOI":"10.3390\/microorganisms14051158","type":"journal-article","created":{"date-parts":[[2026,5,20]],"date-time":"2026-05-20T12:30:51Z","timestamp":1779280251000},"page":"1158","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Biocidal Conditions in Low-Mars-Orbit Can Inactivate Bioburden on External Mars Spacecraft Surfaces and Dust Particles Within a Few Sols"],"prefix":"10.3390","volume":"14","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-3781-5046","authenticated-orcid":false,"given":"Andrew C.","family":"Schuerger","sequence":"first","affiliation":[{"name":"Department of Plant Pathology, University of Florida, Gainesville, FL 32611, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Petra","family":"Schwendner","sequence":"additional","affiliation":[{"name":"Department of Plant Pathology, University of Florida, Gainesville, FL 32611, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lisa","family":"Guan","sequence":"additional","affiliation":[{"name":"Jet Propulsion Laboratory, California Institute of Technology, Pasadena, CA 91109, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jerami","family":"Mennella","sequence":"additional","affiliation":[{"name":"Jet Propulsion Laboratory, California Institute of Technology, Pasadena, CA 91109, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nicholas","family":"Heinz","sequence":"additional","affiliation":[{"name":"Jet Propulsion Laboratory, California Institute of Technology, Pasadena, CA 91109, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9784-6170","authenticated-orcid":false,"given":"Ioannis","family":"Mikellides","sequence":"additional","affiliation":[{"name":"Jet Propulsion Laboratory, California Institute of Technology, Pasadena, CA 91109, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Brian G.","family":"Clement","sequence":"additional","affiliation":[{"name":"Jet Propulsion Laboratory, California Institute of Technology, Pasadena, CA 91109, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,5,20]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"270","DOI":"10.1016\/j.actaastro.2024.05.048","article-title":"NASA\u2019s Capture, Containment, and Return system: Bringing Mars samples to Earth","volume":"223","author":"Sarli","year":"2024","journal-title":"Acta Astronaut."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"104792","DOI":"10.1016\/j.pss.2019.104792","article-title":"Modelling and simulations of particle resuspension and transport for the assessment of terrestrial-borne biological contamination of the samples on the mars 2020 mission","volume":"181","author":"Mikellides","year":"2020","journal-title":"Planet. Space Sci."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"104793","DOI":"10.1016\/j.pss.2019.104793","article-title":"Experiments in particle resuspension and transport for the assessment of terrestrial-borne biological contamination of the samples on the mars 2020 mission","volume":"181","author":"Mikellides","year":"2020","journal-title":"Planet. Space Sci."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"862","DOI":"10.1089\/ast.2022.0048","article-title":"Mars 2020 mission biological return sample contamination control approach and verification","volume":"23","author":"Chen","year":"2023","journal-title":"Astrobiology"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"374","DOI":"10.1016\/j.jsse.2024.04.013","article-title":"The planetary protection strategy of Mars Sample Return\u2019s Earth Return Orbiter mission","volume":"11","author":"Cataldo","year":"2024","journal-title":"J. Space Saf. Eng."},{"key":"ref_6","unstructured":"Clement, B.G. (2025, January 1\u20134). Mars Sample Return Update [Online]. Presented at the National Academies of Sciences, Engineering, and Medicine Event, Washington, DC, USA. Available online: https:\/\/www.nationalacademies.org\/cdn\/materials\/9fba0bb1-c479-4b31-b863-abb044914109."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"887","DOI":"10.1089\/ast.2014.1227","article-title":"A new analysis of Mars \u201cSpecial Regions\u201d: Findings of the Second MEPAG Special Regions Science Analysis Group (SR-SAG2)","volume":"14","author":"Rummel","year":"2014","journal-title":"Astrobiology"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1450","DOI":"10.1089\/ast.2019.2205","article-title":"A Cruise-Phase Microbial Survival model for calculating bioburden reductions on past or future spacecraft throughout their missions with applications to Europa Clipper","volume":"20","author":"Moores","year":"2020","journal-title":"Astrobiology"},{"key":"ref_9","unstructured":"Mikellides, I.G., Heinz, N.A., Mennella, J., and Clement, B.G. (J. Geophys. Res. Planets, 2025). The transmittance of micron-sized abiological Mars simulant particles to ultraviolet radiation, J. Geophys. Res. Planets, submitted."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Sandle, T. (2013). Sterility, Sterilization and Microorganisms. Sterility, Sterilization and Sterility Assurance for Pharmaceuticals, Woodhead Publishing. Woodhead Publishing Series in Biomedicine.","DOI":"10.1533\/9781908818638"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1017\/S1473550420000397","article-title":"Biological safety in the context of backward planetary protection and Mars Sample Return: Conclusions from the Sterilization Working Group","volume":"20","author":"Craven","year":"2021","journal-title":"Int. J. Astrobiol."},{"key":"ref_12","unstructured":"Ratner, B.D., Hoffman, A.S., Schoen, F.J., and Lemons, J.E. (2013). Chapter III. 1.2\u2014Sterilization of Implants and Devices. Biomaterials Science An Introduction to Materials in Medicine, Academic Press. [3rd ed.]."},{"key":"ref_13","unstructured":"(2022). Implementing Planetary Protection Requirements for Spaceflight (Standard No. NASA-STD-8719.27). NASA Technical Standard."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"730","DOI":"10.1089\/ast.2018.1952","article-title":"A Lunar Microbial Survival model for predicting the forward contamination of the Moon","volume":"19","author":"Schuerger","year":"2019","journal-title":"Astrobiology"},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Blachowicz, A., Chiang, A.J., Elsaesser, A., Kalkum, M., Ehrenfreund, P., Stajich, J.E., Torok, T., Wang, C.C.C., and Venkateswaran, K. (2019). Proteomic and metabolomic characteristics of extremophilic fungi under simulated Mars conditions. Front. Microbiol., 10.","DOI":"10.3389\/fmicb.2019.01013"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1093","DOI":"10.1016\/S0032-0633(00)00083-0","article-title":"Martian soil and UV radiation: Microbial viability assessment on spacecraft surfaces","volume":"48","author":"Mancinelli","year":"2000","journal-title":"Planet. Space Sci."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1016\/S0019-1035(03)00200-8","article-title":"Survival of endospores of Bacillus subtilis on spacecraft surfaces under simulated martian environments: Implications for the forward contamination of Mars","volume":"165","author":"Schuerger","year":"2003","journal-title":"Icarus"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1061","DOI":"10.1089\/ast.2021.0141","article-title":"Microbial protocols for Mars spacecraft: 1. Effects of surface texture, low-pressure, and UV irradiation on recovery of microorganisms from surfaces","volume":"22","author":"Schuerger","year":"2022","journal-title":"Astrobiology"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"908","DOI":"10.1089\/ast.2022.0072","article-title":"Microbial protocols for Mars spacecraft: 3. Preparation of uniform and smooth spore monolayers","volume":"23","author":"Schuerger","year":"2023","journal-title":"Astrobiology"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"308","DOI":"10.1038\/nature10344","article-title":"Suppression of the coffee-ring effect by shape-dependent capillary interactions","volume":"476","author":"Yunker","year":"2011","journal-title":"Nature"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1016\/j.mimet.2013.05.003","article-title":"High-density, homogenous endospore monolayer deposition on test surfaces","volume":"94","author":"Noell","year":"2013","journal-title":"J. Microbiol. Methods"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1016\/j.icarus.2007.10.010","article-title":"Slow degradation of ATP in simulated martian environments suggests long residence times for the biosignature molecule on spacecraft surfaces on Mars","volume":"194","author":"Schuerger","year":"2008","journal-title":"Icarus"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1016\/j.icarus.2011.02.017","article-title":"Methane evolution from UV-irradiated spacecraft materials under simulated martian conditions: Implications for the Mars Science Laboratory MSL mission","volume":"213","author":"Schuerger","year":"2011","journal-title":"Icarus"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1016\/j.pss.2017.09.008","article-title":"UV production of methane from surface and sedimenting IDPs on Mars in light of the REMs data and new insights for TGO","volume":"147","author":"Moores","year":"2017","journal-title":"Planet. Space Sci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"A33","DOI":"10.1051\/swsc\/2015035","article-title":"A model to calculate solar radiation fluxes on the Martian surface","volume":"5","author":"Valero","year":"2015","journal-title":"J. Space Weather Space Clim."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"470","DOI":"10.1016\/j.icarus.2008.05.004","article-title":"Mojave Mars simulant-characterization of a new geologic Mars analog","volume":"197","author":"Peters","year":"2008","journal-title":"Icarus"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"113936","DOI":"10.1016\/j.icarus.2020.113936","article-title":"JSC-Rocknest: A large-scale Mojave Mars Simulant (MMS) based soil simulant for in-situ resource utilization water-extraction studies","volume":"351","author":"Clark","year":"2020","journal-title":"Icarus"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1111\/jac.12220","article-title":"What\u2019s normal anyway? Residual plots are more telling than significance tests when checking ANOVA assumptions","volume":"204","author":"Kozak","year":"2018","journal-title":"J. Agron. Crop Sci."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"730","DOI":"10.2134\/agronj2012.0394","article-title":"Multiple comparison procedures\u2014Cutting the Gordian knot","volume":"107","author":"Saville","year":"2015","journal-title":"Agron. J."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1016\/j.icarus.2005.10.008","article-title":"Rapid inactivation of seven Bacillus spp. under simulated Mars UV irradiation","volume":"181","author":"Schuerger","year":"2006","journal-title":"Icarus"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"8147","DOI":"10.1128\/AEM.71.12.8147-8156.2005","article-title":"Survival of spacecraft-associated microorganisms under simulated Martian UV irradiation","volume":"71","author":"Newcombe","year":"2005","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"959","DOI":"10.1128\/AEM.01973-07","article-title":"Effect of shadowing on survival of bacteria under conditions simulating the martian atmosphere and UV radiation","volume":"74","author":"Osman","year":"2008","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/j.pss.2012.07.026","article-title":"Biotoxicity of Mars soils: 1. Dry deposition of analog soils on microbial colonies and survival under Martian conditions","volume":"72","author":"Schuerger","year":"2012","journal-title":"Planet. Space Sci."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"487","DOI":"10.1089\/ast.2011.0738","article-title":"Survival of Bacillus pumilus spores for a prolonged period of time in real space conditions","volume":"12","author":"Vaishampayan","year":"2012","journal-title":"Astrobiology"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1791","DOI":"10.1007\/s43630-024-00632-4","article-title":"Accumulated melanin in molds provides wavelength-dependent UV tolerance","volume":"23","author":"Onoda","year":"2024","journal-title":"Photochem. Photobiol. Sci."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1612","DOI":"10.1111\/1462-2920.13681","article-title":"Melanin is effective in protecting fast and slow growing fungi from various types of ionizing radiation","volume":"19","author":"Pacelli","year":"2017","journal-title":"Environ. Microbiol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"e2201139119","DOI":"10.1073\/pnas.2201139119","article-title":"Organic carbon concentrations in 3.5-billion-year-old lacustrine mudstones of Mars","volume":"119","author":"Stern","year":"2022","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"825","DOI":"10.1089\/ast.2022.0046","article-title":"Planetary protection implementation and verification approach for the Mars 2020 mission","volume":"7","author":"Cooper","year":"2023","journal-title":"Astrobiology"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"37","DOI":"10.3847\/PSJ\/ae38b4","article-title":"A Mars Microbial Survival Model: Calculating Bioburden Reductions for Past Mars Spacecraft to Estimate Forward Contamination on Mars","volume":"7","author":"Bischof","year":"2026","journal-title":"Planet. Sci. J."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/14\/5\/1158\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,5,22]],"date-time":"2026-05-22T04:28:57Z","timestamp":1779424137000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/14\/5\/1158"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,5,20]]},"references-count":39,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2026,5]]}},"alternative-id":["microorganisms14051158"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms14051158","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,5,20]]}}}