Ultraviolet Radiation Sensitivity in Cave Bacteria: Evidence of Adaptation to the Subsurface?


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Ultraviolet Radiation Sensitivity in Cave Bacteria: Evidence of Adaptation to the Subsurface?

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Title:
Ultraviolet Radiation Sensitivity in Cave Bacteria: Evidence of Adaptation to the Subsurface?
Creator:
Snider, Jessica R.
Goin, Caitlin
Miller, Robert V.
Boston, Penelope J.
Northup, Diana E.
Language:
English

Subjects

Subjects / Keywords:
Ultraviolet Radiation Sensitivity ( local )
Cave-Adaptation ( local )
Bacteria ( local )
Subsurface ( local )
Caves ( local )
Genre:
serial ( sobekcm )

Notes

Abstract:
We hypothesize that a reduced capacity to withstand or repair cellular damage from ultraviolet radiation may be present in cave-adapted microorganisms that never experience such conditions. However, a small number of previous studies have shown that some subsurface bacteria do not show greater sensitivity to ultraviolet radiation (UVR) than surface bacteria. To estimate UVR sensitivity in cave bacteria, bacterial isolates were collected from Carlsbad Cavern, New Mexico, U.S.A., and percent survival following exposure to various UVC and UVA radiation doses was determined. Cave bacteria from Left Hand Tunnel in Carlsbad Cavern and surface bacteria from soil and rocks above Carlsbad Cavern were grown on low and high nutrient media then exposed to 0, 10,000 and 20,000 μWs/ cm2 of UVR in a laboratory biological safety cabinet. Incubations were conducted at 15°C or 37ºC, in accordance with the isolates’ natural temperature environments. In addition, DNA repair capacity was estimated by exposing the organisms to various doses of UVC radiation and measuring survivability. Gram status and pigmentation also were determined. Results showed that most of the cave isolates were more sensitive to UVR than the surface isolates, but survivability data suggest that cave microbes retain some of their capacity to repair UV-induced DNA damage. Selection appears to have favored bacteria that can survive in this low nutrient environment, while not maintaining (or paying the cost of maintaining) unneeded traits such as UVR resistance. Cave bacteria appear to have maintained DNA repair capacity, most likely because of the need to repair damage to their DNA from other environmental stressors found in caves.
Original Version:
Vol. 38.

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University of South Florida Library
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University of South Florida
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K26-00014 ( USFLDC: LOCAL DOI )
k26.14 ( USFLDC: LOCAL Handle )

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Available online at www.ijs.speleo.itInternational Journal of Speleology International Journal of Speleology 38 (1) 11-22 Bologna (Italy) January 2009Ultraviolet Radiation Sensitivity in Cave Bacteria: Evidence of Adaptation to the Subsurface?INTRODUCTION Snider J.R., Goin C., Miller R.V., Boston P.J. and Northup D.E. 2009. Ultraviolet Radiation Sensitivity in Cave Bacteria: Evidence of Adaptation to the Subsurface? International Journal of Speleology, 38 (1), 13-22. Bologna (Italy). ISSN 0392-6672. We hypothesize that a reduced capacity to withstand or repair cellular damage from ultraviolet radiation may be present in caveadapted microorganisms that never experience such conditions. However, a small number of previous studies have shown that some subsurface bacteria do not show greater sensitivity to ultraviolet radiation (UVR) than surface bacteria. To estimate UVR sensitivity in cave bacteria, bacterial isolates were collected from Carlsbad Cavern, New Mexico, U.S.A., and percent survival following exposure to various UVC and UVA radiation doses was determined. Cave bacteria from Left Hand Tunnel in Carlsbad Cavern and surface bacteria cm2 of UVR in a laboratory biological safety cabinet. Incubations were conducted at 15C or 37C, in accordance with the isolates’ natural temperature environments. In addition, DNA repair capacity was estimated by exposing the organisms to various doses of UVC radiation and measuring survivability. Gram status and pigmentation also were determined. Results showed that most of the cave isolates were more sensitive to UVR than the surface isolates, but survivability data suggest that cave microbes retain some of their capacity to repair UV-induced DNA damage. Selection appears to have favored bacteria that can survive in this low nutrient environment, while not maintaining (or paying the cost of maintaining) unneeded traits such as UVR resistance. Cave bacteria appear to have maintained DNA repair capacity, most likely because of the need to repair damage to their DNA from other environmental stressors found in caves. Keywords: Ultraviolet radiation sensitivity, cave-adaptation, bacteria, subsurface, caves Received 1 May 2008; Revised 7 September 2008; Accepted 10 September 2008 ., . Available online at www.ijs.speleo.itInternational Journal of Speleology Abstract: 5

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International Journal of Speleology, 38(1), 11-22 Bologna (Italy). January 2009Jessica R. Snider, Caitlin Goin, Robert V. Miller, Penelope J. Boston and Diana E. Northup MATERIALS AND METHODSSite Description and Bacterial Isolation

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International Journal of Speleology, 38(1), 11-22 Bologna (Italy). January 2009Ultraviolet Radiation Sensitivity in Cave Bacteria: Evidence of Adaptation to the Subsurface?UVR Irradiation Studies Pigmentation and Gram Status Determination Statistical Analysis of Data Survival Curve Study S Fig 1. Iron Pool in Left Hand Tunnel, Carlsbad Cavern, Carlsbad, NM. Notice the yellow color of iron pool. Sample Number Location collected CCA2 Iron Pool Water CCB1 Iron Pool Water CCB3 Moonmilk CCB4 Iron Pool Water CCC1 Pool Water CCC2 Moonmilk CCC3 Iron Pool Water CCC4 Pool Water CCD1 Iron Pool Water CCD2 Iron Pool Water CCE1 Swab of Moonmilk CCE2 Moonmilk CCE3 Moonmilk CCE4 Iron Pool Water CCF1 CCF2 CCF3 Table 1. Summary of sampling sites for the 22 cave bacterial isolates used in UVR irradiation study.

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Phylogenetic Analysis of Cave Samples http:// www.bioinformatics-toolkit.or g http://greengenes.lbl.gov/cgi-bin/nph-index.cgi http://www.mbio.ncsu.edu/BioEdit/ BioEdit.html RESULTSUVR Irradiation Studies Surface Area Growth Measurements to Determine Percent Survival Fig 2. Percent survival based on surface area growth, of cave and surface isolates on R2A after exposure to two levels of UVR. Note that percent 2. After a UVR treatment 2 all tested isolates after exposure to UVR in an open (no lid on) media plate in a biological safety cabinet. Jessica R. Snider, Caitlin Goin, Robert V. Miller, Penelope J. Boston and Diana E. NorthupInternational Journal of Speleology, 38(1), 11-22 Bologna (Italy). January 2009

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P P CFU Measurements to Determine Percent Survival P Fig 3. Percent survival, based on surface area growth, of cave and surface isolates on LB after exposure to two levels of UVR. Note that after UVR 2 2 of UVR, the surface isolates actually had an increase in percent survival. Percent survival higher than 2 This information was calculated from an average of all tested isolates after exposure to UVR in an open (no lid on) media plate in a biological safety cabinet. Ultraviolet Radiation Sensitivity in Cave Bacteria: Evidence of Adaptation to the Subsurface?International Journal of Speleology, 38(1), 11-22 Bologna (Italy). January 2009

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Cellular Characteristics (Pigmentation and Gram Status) Fig 4. Percent survival, based on colony forming unit measurements, of cave and surface isolates on LB and R2A after two levels of UVR. These and surface isolates had lower percent survival amounts when grown on R2A, the low nutrient medium, than when grown on LB, the high nutrient isolates after exposure to UVR in an open (no lid on) media plate in a biological safety cabinet. Jessica R. Snider, Caitlin Goin, Robert V. Miller, Penelope J. Boston and Diana E. NorthupInternational Journal of Speleology, 38(1), 11-22 Bologna (Italy). January 2009

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Survival following various doses of UVC radiation Phylogenetic Analysis of Cave Samples Actinobacteria, Proteobacteria Proteobacteria Alphaproteobacteria Betaproteobacteria Gammproteobacteria Actinobacteria Knoellia subterranea Tetrasphaera Microbacterium Microbacterium phyllosphaerae, a Rhodococcus Rhodococcus Proteobacteria Alpha-, BetaGammaproteobacteria Pseudomonas Xanthomonas Pseudomonas Fig 5. Pigmentation levels of cave and rurface isolates. Pigmentation level was based on colony coloration when grown on R2A. Low pigmentation meant no pigment was noticeable. Medium (mid) pigmentation meant that colonies had a white or tan opaqueness, while high pigmentation meant that colonies had bright, solid colors, such as purple, pink, yellow, or white. Pigmentation / sensitivity level # of clones with 5 9 8 0 Table 2. Correlation of Pigmentation and Sensitivity in Surface and Cave Isolates. Sensitivity when determined by CFU measurements cm2 when grown on R2A. Sensitivity when determined by surface 2 when grown on R2A. Note that isolates with high levels of pigmentation varied in whether they were sensitive or resistant to UVR, but no isolates with low levels of pigmentation were resistant (i.e. not sensitive) to UVR.Ultraviolet Radiation Sensitivity in Cave Bacteria: Evidence of Adaptation to the Subsurface?International Journal of Speleology, 38(1), 11-22 Bologna (Italy). January 2009

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Chitinimonas DISCUSSION Knoellia subterranea Actinobacteria Proteobacteria Fig 6. Survival rates following various doses of UVC radiation. Data Strain Percent survival at 100 J/m2SUVSurface B2 49 .007 B3 27 .013 Cave B1 12 .021 B4 10 .029 C3 1 .056 E3 3 .035 F3 13 .020 Table 3. Sensitivity of various strains to UVC irradiation. UV 2 using the formula of Simonson et al. (1990). Jessica R. Snider, Caitlin Goin, Robert V. Miller, Penelope J. Boston and Diana E. NorthupInternational Journal of Speleology, 38(1), 11-22 Bologna (Italy). January 2009

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Fig 7. Phylogram of cave bacterial isolates. Only sequences with >650 bp were included. Phylogenetic analysis was carried out using parsimonious (heuristic) searches, with robustness determined by 1000 replicate bootstrap analysis. Ultraviolet Radiation Sensitivity in Cave Bacteria: Evidence of Adaptation to the Subsurface?International Journal of Speleology, 38(1), 11-22 Bologna (Italy). January 2009

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full potential in ACKNOWLEDGEMENTS Jessica R. Snider, Caitlin Goin, Robert V. Miller, Penelope J. Boston and Diana E. NorthupInternational Journal of Speleology, 38(1), 11-22 Bologna (Italy). January 2009

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REFERENCES Gapped BLAST and PSI-BLAST: a new generation of protein database search program. 25 Survival of subsurface microorganisms exposed to UV radiation and hydrogen peroxide 59 Bacterial sensitivity to UV light as a model for ionizing radiation resistance. Journal of 18 New screening software shows that most recent large 16S rRNA gene clone libraries contain chimeras. 72 The impact of host rock geochemistry on bacterial community structure in oligotrophic cave environments. International Journal 36 RecA expression in response to solar UVR in the marine bacterium Vibrio natreiegens 42 The mechanism of action of DNA photolyases. 5 Biological effects of high ultraviolet radiation on early Earth-A theoretical evaluation. 193 Cave Life: Evolution and Ecology. stalactite Cave (Israel) and way of its control. 94 Light as an Extreme Environment. The Prokaryotes: a Handbook on the Biology of Bacteria Sensitivity of selected bacterial species to UV radiation. 30 Microbial th Knoellia sinensis gen. nov., sp. nov. and Knoellia subterranean sp. nov., two novel actinobacteria isolated from a cave. 52 Cave Minerals of the World (2nd edition). Physiological effects of nearultraviolet radiation on bacteria. 7 Solar-UV Actions on Living Cells. Molecular cloning and characterization of the recA gene of Pseudomonas aeruginosa, 163 The effects of continuous darkness on cave ecology and cavernicolus evolution. Subterranean Ecosystems Student Handbook Role of carotenoid pigments in radio-resistant micrococci. 20 Functions of carotenoid pigments in non-photosynthetic bacteria. 184 Bacterial response to solar ultraviolet light. , 65: recA: The gene and its protein product. Encylopedia of Microbiology 2nd Edition, Vol.4 Life under conditions of high irradiation Microbial Life in Extreme Environments. On the nature of bacterial communities in Four Windows Cave, El Malpais National Monument, New Mexico, USA. 19 Evidence for geomicrobiological interactions in Guadalupe (NM) Caves. 62 Bioenergetics of Ceuthophilus camel crickets from Carlsbad Caverns National Park. 106A Photosynthesis below the surface in a cryptic microbial mat. 1 Ultraviolet Radiation Sensitivity in Cave Bacteria: Evidence of Adaptation to the Subsurface?International Journal of Speleology, 38(1), 11-22 Bologna (Italy). January 2009

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Inducible UV repair potential of Pseudomonas aeruginosa PAO, 136 Sunlight ultraviolet and bacterial DNA base ratios. 170 Archaen stromatolites: Evidence of the Earth’s earliest benthos Earth’s Earliest Biosphere Alternative repair pathways for UV-induced DNA damage20: Jessica R. Snider, Caitlin Goin, Robert V. Miller, Penelope J. Boston and Diana E. NorthupInternational Journal of Speleology, 38(1), 11-22 Bologna (Italy). January 2009


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