Survivability of Soil and Permafrost Microbial Communities after Irradiation with Accelerated Electrons under Simulated Martian and Open Space Conditions
Abstract
:1. Introduction
2. Materials and Methods
2.1. Objects of Study
2.2. Preparation of Samples for Irradiation with Accelerated Electrons
2.3. Description of the Climatic Chamber
2.4. Irradiation of Samples with Accelerated Electrons
2.5. Culturing of Microbial Communities
2.6. Accounting for the Total Numbers of Prokaryotes
2.7. Multisubstrate Testing of Integral Metabolic Activity and Functional Diversity of Microbial Communities (MST)
2.8. Identification of Bacterial Isolates
2.9. Investigation of the Physiological Characteristics of Isolates
2.10. Irradiation of Pure Bacterial Cultures with Gamma Radiation
3. Results and Discussion
3.1. Bacteria Abundance in the Samples
3.2. Metabolic Activity of Microbial Communities
3.3. Taxonomic Affiliation and Physiological Characteristics of Bacterial Isolates
3.4. Irradiation of Pure Bacterial Cultures with Accelerated Electrons under Simulated Extraterrestrial Conditions
3.5. Survivability of Pure Bacterial Cultures under Gamma Irradiation
3.6. Implications for Habitability Assessment
4. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
Appendix A
Strain—GenBank Accession Number | Primers Used for the Amplification | Primers Used for the Sequencing |
---|---|---|
KBP.AS.531—MH050938 | 63F+1387R | 1100R |
KBP.AS.532—MH050939 | 27F+537R | 537R |
KBP.AS.340—MH050940 | 63F+1387R | 1100R |
KBP.AS.341—MH050941 | 63F+1387R | 1100R |
KBP.AS.342—MH050942 | 63F+1387R | 1100R |
KBP.AS.343—MH050943 | 63F+1387R | 1100R |
KBP.AS.344—MH050944 | 63F+1387R | 1100R |
KBP.AS.345—MH050945 | 63F+1387R | 1100R; 537R |
KBP.AS.346—MH050946 | 63F+1387R | 1100R |
KBP.AS.347—MH050947 | 63F+1387R | 1100R |
KBP.AS.298—MH050948 | 63F+1387R | 1100R |
KBP.AS.299—MH050949 | 63F+1387R | 1100R |
KBP.AS.300—MH050950 | 63F+1387R | 1100R |
KBP.AS.533—MH050951 | 63F+1387R | 1100R |
KBP.AS.301—MH050952 | 63F+1387R | 1100R |
KBP.AS.302—MH050953 | 63F+1387R | 1100R |
KBP.AS.303—MH050954 | 63F+1387R | 1100R |
KBP.AS.534—MH050955 | 27F+Un1492R | 1100R |
KBP.AS.297—MH050956 | 63F+1387R | 1100R |
KBP.AS.321—MH050957 | 63F+1387R | 1100R; 537R |
KBP.AS.322—MH050958 | 63F+1387R | 1100R |
KBP.AS.323—MH050959 | 63F+1387R | 1100R |
KBP.AS.324—MH050960 | 63F+1387R | 1100R |
KBP.AS.325—MH050961 | 63F+1387R | 1100R |
KBP.AS.535—MH050962 | 63F+1387R | 1100R |
KBP.AS.536—MH050963 | 63F+1387R | 1100R |
KBP.AS.326—MH050964 | 63F+1387R | 1100R; 537R |
KBP.AS.317—MH050965 | 63F+1387R | 1100R |
KBP.AS.319—MH050966 | 63F+1387R | 1100R |
KBP.AS.320—MH050967 | 63F+1387R | 1100R |
KBP.AS.537—MH050968 | 63F+1387R | 1100R |
Appendix B
SN2, TPC | SN2, 10 kGy | SN2, 100 kGy |
---|---|---|
Arthrobacter | Arthrobacter | Arthrobacter |
Saccharothrix | ||
Phenylobacterium | ||
Cryobacterium | ||
Streptomyces | ||
Microbacterium | ||
Micrococcus | Micrococcus | |
Sphingoaurantiacus | ||
Bacillus | ||
Spirosoma | Spirosoma | |
Rufibacter | Rufibacter | |
Planomicrobium | ||
Massilia | ||
Microvirga | ||
Pontibacter |
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Sample | SN2 | M-1/91 | |
---|---|---|---|
Attribute | |||
pH | 8.11 | 7.51 | |
NO2−, mg/kg | Traces | Traces | |
NO3−, mg/kg | 1.03 | 0.89 | |
NH4+, mg/kg | 4.12 | 3.34 | |
Cl−, mg/kg | 58.15 | 49.84 | |
CO32–, mg/kg | 330.41 | 129.29 | |
Na+, mg/kg | 512.7 | 87.57 | |
Mn2+, mg/kg | 1348.2 | 3.23 | |
Mg2+, mg/kg | 136.46 | 170.4 | |
K+, mg/kg | 877.5 | 40.47 | |
Fe2++Fe3+, mg/kg | 4.35 | 29.55 | |
Total organic carbon, % | 1.27 | 0.32 |
Sample | Consumption of Substrates of Different Groups, Relative Units | |||||||
---|---|---|---|---|---|---|---|---|
Pentoses | Hexoses | Oligoses | Alcohols | Amino Acids | Salts of Carboxylic Acids | Polymers | Amides, Amines, Nucleosides | |
SN2, Control | 526 | 3950 | 5340 | 4910 | 6186 | 3894 | 2654 | 124 |
SN2, TPC | 544 | 3972 | 5294 | 4862 | 6268 | 3754 | 2716 | 132 |
SN2, 10 kGy | 0 | 0 | 0 | 0 | 0 | 0 | 122 | 0 |
SN2, 100 kGy | 0 | 0 | 0 | 0 | 0 | 0 | 114 | 0 |
M-1/91, Control | 2150 | 1420 | 1912 | 2562 | 5670 | 4318 | 3642 | 22 |
M-1/91, 100 kGy | 0 | 0 | 0 | 0 | 0 | 0 | 146 | 0 |
Sample | Strain—Genbank Accession Number | The Most Closely Related Sequences in Genbank—Similarity, % | Taxonomic Affiliation |
---|---|---|---|
SN2, TPC | KBP.AS.531 MH050938 | JX949673 Arthrobacter sp.—100 | Arthrobacter sp. 1 |
NR_026198 Arthrobacter agilis—99.5 | |||
NR_148833 Arthrobacter echini—99.3 | |||
SN2, TPC | KBP.AS.532 MH050939 | JQ419609 Saccharothrix sp.—99.8 | Saccharothrix sp. |
NR_109447 Saccharothrix ecbatanensis—99.5 | |||
NR_109103 Saccharothrix hoggarensis—99.5 | |||
SN2, TPC | KBP.AS.340 MH050940 | KJ578028 Uncultured bacterium clone—99.9 | Phenylobacterium sp. |
KT191026 Phenylobacterium panacis—99.5 | |||
NR_117783 Phenylobacterium muchangponense—99.5 | |||
SN2, TPC | KBP.AS.341 MH050941 | DQ177485 Microbacteriaceae bacterium—99.6 | Cryobacterium sp. |
KR857373 Cryobacterium sp.—99.4 | |||
FR691394 Cryobacterium sp.—99.4 | |||
NR_108605 Cryobacterium arcticum—99.4 | |||
JX205201 Cryobacterium psychrotolerans—99.2 | |||
SN2, TPC | KBP.AS.342 MH050942 | KY820858 Streptomyces fulvissimus—99.3 | Streptomyces sp. |
AJ781354 Streptomyces mediolani—99.3 | |||
SN2, TPC | KBP.AS.343 MH050943 | NR_119270 Microbacterium saperdae—100 | Microbacterium sp. |
NR_025405 Microbacterium phyllosphaerae—100 | |||
SN2, TPC | KBP.AS.344 MH050944 | GQ232449 Bacterium RK91_tank—100 | Micrococcus sp. 2 |
JN378531 Micrococcus luteus—99.9 | |||
NR_134088 Micrococcus aloeverae—99.7 | |||
NR_116578 Micrococcus yunnanensis—99.6 | |||
SN2, TPC | KBP.AS.345 MH050945 | DQ906916 Uncultured bacterium clone—99.4 | Sphingoaurantiacus sp. |
NR_147725 Sphingoaurantiacus polygranulatus—96.8 | |||
NR_148321 Sphingomonas chloroacetimidivorans—95.4 | |||
KT321369 Sphingoaurantiacus capsulatus—95.3 | |||
SN2, TPC | KBP.AS.346 MH050946 | JX840970 Arthrobacter oxydans—100 | Arthrobacter sp. 3 |
NR_108849 Arthrobacter siccitolerans—99.7 | |||
NR_026192 Arthrobacter polychromogenes—99.6 | |||
SN2, TPC | KBP.AS.347 MH050947 | NR_117474 Bacillus frigoritolerans—100 | Bacillus sp. |
NR_114919 Bacillus simplex—100 | |||
SN2, 10 kGy | KBP.AS.298 MH050948 | NR_113978 Spirosoma rigui—99.8 | Spirosoma sp. 4 |
EF507901 Spirosoma aquatica—99.8 | |||
SN2, 10 kGy | KBP.AS.299 MH050949 | AB637009 Uncultured bacterium clone—100 | Rufibacter immobilis |
HG316123 Rufibacter immobilis—99 | |||
CP012645 Rufibacter tibetensis—97.8 | |||
SN2, 10 kGy | KBP.AS.300 MH050950 | NR_042469 Arthrobacter phenanthrenivorans—100 | Arthrobacter sp. 3 |
NR_117356 Arthrobacter cryotolerans—100 | |||
NR_041546 Arthrobacter humicola—100 | |||
SN2, 10 kGy | KBP.AS.533 MH050951 | KY386623 Arthrobacter sp.—100 | Arthrobacter sp. 1 |
NR_026198 Arthrobacter agilis—100 | |||
NR_148833 Arthrobacter echini—99.6 | |||
SN2, 10 kGy | KBP.AS.301 MH050952 | HQ860629 Uncultured bacterium clone—100 | Planomicrobium sp. 5 |
GQ140340 Planomicrobium okeanokoites—99.9 | |||
NR_116601 Planomicrobium flavidum—99.7 | |||
SN2, 10 kGy | KBP.AS.302 MH050953 | HQ860629 Uncultured bacterium clone—100 | Planomicrobium sp. 5 |
GQ140340 Planomicrobium okeanokoites—99.9 | |||
NR_116601 Planomicrobium flavidum—99.7 | |||
SN2, 10 kGy | KBP.AS.303 MH050954 | FR675946 Uncultured bacterium clone—99.5 | Massilia sp. |
NR_117040 Massilia consociata—99.0 | |||
NR_042502 Massilia aurea—98.4 | |||
NR_126273 Massilia kyonggiensis—98.4 | |||
SN2, 10 kGy | KBP.AS.534 MH050955 | NR_134088 Micrococcus aloeverae—99.8 | Micrococcus sp. 2 |
NR_116578 Micrococcus yunnanensis—99.8 | |||
SN2, 100 kGy | KBP.AS.297 MH050956 | NR_113978 Spirosoma rigui—99.8 | Spirosoma sp. 4 |
EF507901 Spirosoma aquatica—99.8 | |||
SN2, 100 kGy | KBP.AS.321 MH050957 | AB637009 Uncultured bacterium clone—99.7 | Rufibacter sp. |
JF417863 Uncultured bacterium clone—97.9 | |||
HG316124 Rufibacter immobilis—96.8 | |||
NR_116350 Rufibacter tibetensis—96.3 | |||
SN2, 100 kGy | KBP.AS.322 MH050958 | HQ910259 Uncultured bacterium clone—99.6 | Microvirga sp. |
JX504809 Microvirga vignae—98.7 | |||
NR_114298 Microvirga aerilata—98.7 | |||
SN2, 100 kGy | KBP.AS.323 MH050959 | KC354446 Arthrobacter sp.—100 | Arthrobacter sp. 3 |
JX840970 Arthrobacter oxydans—100 | |||
NR_108849 Arthrobacter siccitolerans—99.7 | |||
SN2, 100 kGy | KBP.AS.324 MH050960 | KX247636 Microvirga soli—99.7 | Microvirga soli |
JF295810 Uncultured bacterium clone—99 | |||
HF954468 Microvirga sp.—98 | |||
NR_104766 Microvirga subterranea—97.9 | |||
SN2, 100 kGy | KBP.AS.325 MH050961 | NR_042252 Arthrobacter parietis—100 | Arthrobacter sp. |
KP125973 Arthrobacter subterraneus—100 | |||
SN2, 100 kGy | KBP.AS.535 MH050962 | FR691450 Pontibacter sp.—99.1 | Pontibacter sp. |
NR_148858 Pontibacter amylolyticus—98.1 | |||
NR_116853 Pontibacter salisaro—97.9 | |||
SN2, 100 kGy | KBP.AS.536 MH050963 | KX247636 Microvirga soli—99.4 | Microvirga sp. |
NR_044563 Microvirga guangxiensis—99.1 | |||
SN2, 100 kGy | KBP.AS.326 MH050964 | AJ863207 Uncultured bacterium clone—99 | Pontibacter sp. |
KX350156 Pontibacter sp.—99.0 | |||
JN037908 Uncultured Bacteroidetes bacterium—98.2 | |||
NR_133822 Pontibacter deserti—97.5 | |||
NR_109067 Pontibacter populi—96.3 | |||
M-1/91, 100 kGy | KBP.AS.317 MH050965 | KJ000846 Brevundimonas sp.—99.9 | Brevundimonas sp. |
NR_116722 Brevundimonas naejangsanensis—99.9 | |||
NR_113602 Brevundimonas diminuta—99.7 | |||
M-1/91, 100 kGy | KBP.AS.319 MH050966 | NR_114986 Microbacterium maritypicum—100 | Microbacterium sp. 7 |
KT899483 Microbacterium oxydans—100 | |||
M-1/91, 100 kGy | KBP.AS.320 MH050967 | NR_114986 Microbacterium maritypicum—100 | Microbacterium sp. 7 |
KT899483 Microbacterium oxydans—100 | |||
M-1/91, 100 kGy | KBP.AS.537 MH050968 | HM811712 Uncultured bacterium—99.5 | Stenotrophomonas rhizophila |
NR_121739 Stenotrophomonas rhizophila—99.2 | |||
LT906480 Stenotrophomonas maltophilia—97.9 |
Sample | Strain | Taxonomic Affiliation | Temperature Limits of Growth, °C | pH-range of Growth | Maximum Salt Concentrations at Which Growth Is Possible, % | |||
---|---|---|---|---|---|---|---|---|
NaCl | KCl | MgSO4 | NaHCO3 | |||||
SN2, TPC | KBP.AS.531 | Arthrobacter sp. | 2–37 | 5–9 | 2 | 2 | 15 | 0 |
SN2, TPC | KBP.AS.532 | Saccharothrix sp. | 10–37 | 4–12 | 2 | 5 | 20 | 0 |
SN2, TPC | KBP.AS.340 | Phenylobacterium sp. | 10–37 | 6–12 | 0 | 0 | 5 | 0 |
SN2, TPC | KBP.AS.341 | Cryobacterium sp. | 2–37 | 7–11 | 20 | 15 | 20 | 0 |
SN2, TPC | KBP.AS.342 | Streptomyces sp. | 10–45 | 4–12 | 10 | 10 | 20 | 5 |
SN2, TPC | KBP.AS.343 | Microbacterium sp. | 10–37 | 4–11 | 10 | 15 | 20 | 0 |
SN2, TPC | KBP.AS.344 | Micrococcus sp. | 10–37 | 5–8 | 0 | 5 | 0 | 0 |
SN2, TPC | KBP.AS.346 | Arthrobacter sp. | 2–50 | 6–10 | 0 | 0 | 2 | 0 |
SN2, TPC | KBP.AS.347 | Bacillus sp. | 2–37 | 5–8 | 0 | 5 | 0 | 0 |
SN2, 10 kGy | KBP.AS.298 | Spirosoma sp. | 10–37 | 5–12 | 20 | 15 | 20 | 0 |
SN2, 10 kGy | KBP.AS.299 | Rufibacter immobilis | 2–37 | 6–8 | 0 | 0 | 2 | 0 |
SN2, 10 kGy | KBP.AS.300 | Arthrobacter sp. | 2–37 | 6–8 | 0 | 0 | 2 | 0 |
SN2, 10 kGy | KBP.AS.533 | Arthrobacter sp. | 10–37 | 4–9 | 10 | 15 | 15 | 0 |
SN2, 10 kGy | KBP.AS.301 | Planomicrobium sp. | 2–37 | 5–12 | 0 | 0 | 15 | 0 |
SN2, 10 kGy | KBP.AS.302 | Planomicrobium sp. | 2–37 | 6–12 | 0 | 0 | 15 | 0 |
SN2, 10 kGy | KBP.AS.303 | Massilia sp. | 10–37 | 5–8 | 0 | 0 | 0 | 0 |
SN2, 10 kGy | KBP.AS.534 | Micrococcus sp. | 10–37 | 5–12 | 20 | 15 | 20 | 0 |
SN2, 100 kGy | KBP.AS.297 | Spirosoma sp. | 10–37 | 7–12 | 0 | 0 | 0 | 2 |
SN2, 100 kGy | KBP.AS.323 | Arthrobacter sp. | 4–37 | 8–12 | 5 | 0 | 0 | 2 |
SN2, 100 kGy | KBP.AS.324 | Microvirga sp. | 4–37 | 7–12 | 10 | 15 | 20 | 0 |
SN2, 100 kGy | KBP.AS.325 | Arthrobacter sp. | 2–50 | 5–12 | 0 | 5 | 15 | 0 |
M-1/91, 100 kGy | KBP.AS.317 | Brevundimonas sp. | 10–37 | 5–12 | 20 | 15 | 20 | 0 |
M-1/91, 100 kGy | KBP.AS.319 | Microbacterium sp. | 10–37 | 5–8 | 2 | 2 | 2 | 0 |
M-1/91, 100 kGy | KBP.AS.320 | Microbacterium sp. | 4–50 | 7–12 | 0 | 0 | 2 | 0 |
M-1/91, 100 kGy | KBP.AS.537 | Stenotrophomonas rhizophila | 2–37 | 6–11 | 0 | 0 | 5 | 2 |
Sample | Strain Number | Taxonomic Affiliation |
---|---|---|
SN2, TPC | KBP.AS.341 | Cryobacterium sp. |
SN2, TPC | KBP.AS.343 | Microbacterium sp. |
SN2, TPC | KBP.AS.347 | Bacillus sp. |
SN2, 10 kGy | KBP.AS.301 | Planomicrobium sp. |
SN2, 100 kGy | KBP.AS.323 | Arthrobacter sp. |
SN2, 100 kGy | KBP.AS.324 | Microvirga sp. |
M-1/91, 100 kGy | KBP.AS.319 | Microbacterium sp. |
SN 1 | SN_T60 | Kocuria rosea |
SN 1 | SN_T61 | Arthrobacter polychromogenes |
The strain obtained from the VKM collection | VKM B-1422T | Deinococcus radiodurans |
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Cheptsov, V.; Vorobyova, E.; Belov, A.; Pavlov, A.; Tsurkov, D.; Lomasov, V.; Bulat, S. Survivability of Soil and Permafrost Microbial Communities after Irradiation with Accelerated Electrons under Simulated Martian and Open Space Conditions. Geosciences 2018, 8, 298. https://doi.org/10.3390/geosciences8080298
Cheptsov V, Vorobyova E, Belov A, Pavlov A, Tsurkov D, Lomasov V, Bulat S. Survivability of Soil and Permafrost Microbial Communities after Irradiation with Accelerated Electrons under Simulated Martian and Open Space Conditions. Geosciences. 2018; 8(8):298. https://doi.org/10.3390/geosciences8080298
Chicago/Turabian StyleCheptsov, Vladimir, Elena Vorobyova, Andrey Belov, Anatoly Pavlov, Denis Tsurkov, Vladimir Lomasov, and Sergey Bulat. 2018. "Survivability of Soil and Permafrost Microbial Communities after Irradiation with Accelerated Electrons under Simulated Martian and Open Space Conditions" Geosciences 8, no. 8: 298. https://doi.org/10.3390/geosciences8080298