Abstract
It has been suggested that the cryosphere is a new biome uniquely dominated by microorganisms, although the ecological characteristics of these cold-adapted bacteria are not well understood. We investigated the vertical variation with depth of the proportion of pigmented bacteria recovered from an ice core drilled in the Yuzhufeng Glacier, Tibetan Plateau. A total of 25,449 colonies were obtained from 1250 ice core sections. Colonies grew on only one-third of the inoculated Petri dishes, indicating that although the ice core harbored abundant culturable bacteria, bacteria could not be isolated from every section. Four phyla and 19 genera were obtained; Proteobacteria formed the dominant cluster, followed by Actinobacteria, Bacteroidetes and Firmicutes. The proportion of pigmented bacteria increased with depth from 79 to 95% and yellow-colored colonies predominated throughout the ice core, making up 47% of all the colonies. Pigments including α- and β-carotene, diatoxanthin, peridinin, zea/lutein, butanoyloxy, fucoxanthin and fucoxanthin were detected in representative colonies with α-carotene being the dominant carotenoid. To the best of our knowledge, this is the highest resolution study of culturable bacteria in a deep ice core reported to date.
Similar content being viewed by others
References
Amato P, Hennebelle R, Magand O, Sancelme M, Delort A-M, Barbante C, Boutron C, Ferrari C (2007) Bacterial characterization of the snow cover at Spitzberg, Svalbard. FEMS Microbiol Ecol 59:255–264
Anesio AM, Laybourn-Parry J (2012) Glaciers and ice sheets as a biome. Trends Ecol Evol 27:219–225
Antony R, Krishnan KP, Laluraj CM, Thamban M, Dhakephalkar PK, Engineer AS, Shivaji S (2012) Diversity and physiology of culturable bacteria associated with a coastal Antarctic ice core. Microbiol Res 167:372–380
Bakermans C, Tsapin AI, Souza-Egipsy V, Gilichinsky DA, Nealson KH (2003) Reproduction and metabolism at −10 °C of bacteria isolated from Siberian permafrost. Environ Microbiol 5:321–326
Borić M, Danevčič T, Stopar D (2011) Prodigiosin from Vibrio sp. DSM 14379; a new UV-protective pigment. Microb Ecol 62:528–536
Bowman JP, McCammon SA, Brown MV, Nichols DS, McMeekin TA (1997) Diversity and association of psychrophilic bacteria in Antarctic sea ice. Appl Environ Microbiol 63:3068–3078
Carpenter EJ, Lin SJ, Capone DG (2000) Bacterial activity in South Pole snow. Appl Environ Microbiol 66:4514–4517
Chattopadhyay MK (2006) Mechanism of bacterial adaptation to low temperature. J Biosci (Bangalore) 31:157–165
Christner BC, Mosley-Thompson E, Thompson LG, Zagorodnov V, Sandman K, Reeve JN (2000) Recovery and identification of viable bacteria immured in glacial ice. Icarus 144:479–485
Christner BC, Mosley-Thompson E, Thompson LG, Reeve JN (2001) Isolation of bacteria and 16S rDNAs from Lake Vostok accretion ice. Environ Microbiol 3:570–577
Christner BC, Mosley-Thompson E, Thompson LG, Reeve JN (2003) Bacterial recovery from ancient glacial ice. Environ Microbiol 5:433–436
D’Elia T, Veerapaneni R, Rogers SO (2008) Isolation of microbes from Lake Vostok accretion ice. Appl Environ Microbiol 74:4962–4965
Dillon JG, Miller SR, Castenholz RW (2003) UV-acclimation responses in natural populations of cyanobacteria (Calothrix sp.). Environ Microbiol 5:473–483
Finegold L (1996) Molecular and biophysical aspects of adaptation of life to temperatures below the freezing point. Adv Space Res 18(12):87–95
Foght J, Aislabie J, Turner S, Brown CE, Ryburn J, Saul DJ, Lawson W (2004) Culturable bacteria in subglacial sediments and ice from two Southern Hemisphere glaciers. Microb Ecol 47:329–340
Fong NJC, Burgess ML, Barrow KD, Glenn DR (2001) Carotenoid accumulation in the psychrotrophic bacterium Arthrobacter agilis in response to thermal and salt stress. Appl Microbiol Biotechnol 56:750–756
Katayama T, Tanaka M, Moriizumi J, Nakamura T, Brouchkov A, Douglas TA, Fukuda M, Tomita F, Asano K (2007) Phylogenetic analysis of bacteria preserved in a permafrost ice wedge for 25,000 years. Appl Environ Microbiol 73:2360–2363
Lane DJ (1991) 16S/23S rRNA Sequencing. nucleic acid techniques in bacterial systematics. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–175
Lin J, Zhang XF, An LZ, Ya TD, Li ZQ, Xu SJ (2008) Study of the diversity and depth distribution of bacteria isolated from the core of the glacier no. 1 at the headwaters of the Uriimqi river, Tianshan Mountains. J Glaciol Geocryol 30:1033–1040
Liu YQ, Yao TD, Jiao NZ, Kang SC, Huang SJ, Li Q, Wang KJ, Liu XB (2008) Culturable bacteria in glacial meltwater at 6,350 m on the East Rongbuk Glacier, Mount Everest. Extremophiles 13:89–99
Liu YQ, Yao TD, Xu BL, Jiao NZ, Luo T, Wu GJ, Zhao HB, Shen L, Liu XB (2013) Bacterial abundance vary in Muztagata ice core and respond to climate and environment change in the past hundred years. Quat Sci 33:19–25
Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964
Ma XJ, Liu W, Hou SG, Chen T, Qin DH (2009a) Culturable bacteria in snow pits of different type glaciers: diversity and relationship with environment. J Glaciol Geocryol 31:483–489
Ma XJ, Liu W, Hou SG, Chen T, Qin DH (2009b) Bacterial diversity and community at Yulong Mountains and their relationship to climatic and environmental changes. J Lanzhou Univ Nat Sci 45:94–100
Margesin R, Miteva V (2011) Diversity and ecology of psychrophilic microorganisms. Res Microbiol 162:346–361
Miteva VI, Brenchley JE (2005) Detection and isolation of ultrasmall microorganisms from a 120,000-year-old Greenland glacier ice core. Appl Environ Microbiol 71:7806–7818
Miteva VI, Sheridan PP, Brenchley JE (2004) Phylogenetic and physiological diversity of microorganisms isolated from a deep Greenland glacier ice core. Appl Environ Microbiol 70:202–213
Møller AK, Søborg DA, Abu Al-Soud W, Sørensen SJ, Kroer N (2013) Bacterial community structure in High-Arctic snow and freshwater as revealed by pyrosequencing of 16S rRNA genes and cultivation. Polar Res 32:130–137
Mykytczuk NCS, Foote SJ, Omelon CR, Southam G, Greer CW, Whyte LG (2013) Bacterial growth at −15 °C; molecular insights from the permafrost bacterium Planococcus halocryophilus Or1. ISME J 7:1211–1226
Ponder MA, Gilmour SJ, Bergholz PW, Mindock CA, Hollingsworth R, Thomashow MF, Tiedje JM (2005) Characterization of potential stress responses in ancient Siberian permafrost psychroactive bacteria. FEMS Microbiol Ecol 53:103–115
Remias D, Albert A, Lüetz C (2010) Effects of realistically simulated, elevated UV irradiation on photosynthesis and pigment composition of the alpine snow alga Chlamydomonas nivalis and the arctic soil alga Tetracystis sp. (Chlorophyceae). Photosynthetica 48:269–277
Rivkina EM, Friedmann EI, McKay CP, Gilichinsky DA (2000) Metabolic activity of permafrost bacteria below the freezing point. Appl Environ Microbiol 66:3230–3233
Russell NJ (2000) Toward a molecular understanding of cold activity of enzymes from psychrophiles. Extremophiles 4:83–90
Schmid H, Bauer F, Stich HB (1998) Determination of algal biomass with HPLC pigment analysis from lakes of different trophic state in comparison to microscopically measured biomass. J Plankton Res 20:1651–1661
Shen L, Yao TD, Xu BQ, Wang H, Jiao NZ, Kang SC, Liu XB, Liu YQ (2012) Variation of culturable bacteria along depth in the East Rongbuk ice core, Mt. Everest. Geosci Front 3:327–334
Shen L, Liu YQ, Yao TD, Wang NL, Xu BQ, Jiao NZ, Liu HC, Zhou YG, Liu XB, Wang YN (2013) Dyadobacter tibetensis sp. nov., isolated from glacial ice core. Int J Syst Evol Microbiol 63:3636–3639
Shen L, Yao TD, Liu YQ, Jiao NZ, Kang SC, Xu BQ, Zhang SH (2014) Downward-shifting temperature range for the growth of snow-bacteria on glaciers of the Tibetan Plateau. Geomicrobiol J 31:779–787
Shivaji S, Prakash JSS (2010) How do bacteria sense and respond to low temperature? Arch Microbiol 192:85–95
Simon C, Wiezer A, Strittmatter AW, Daniel R (2009) Phylogenetic diversity and metabolic potential revealed in a glacier ice metagenome. Appl Environ Microbiol 75:7519–7526
Sommaruga R, Casamayor EO (2009) Bacterial ‘cosmopolitanism’ and importance of local environmental factors for community composition in remote high-altitude lakes. Freshw Biol 54:994–1005
Suzuki KI, Sasaki J, Uramoto M, Nakase T, Komagata K (1997) Cryobacterium psychrophilum gen. nov., sp. nov., nom. rev., comb. nov., an obligately psychrophilic Actinomycete to accommodate “Curtobacterium psychrophilum” Inoue and Komagata 1976. Int J Syst Evol Microbiol 47:474–478
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Várkonyi Z, Masamoto K, Debreczeny M, Zsiros O, Ughy B, Gombos Z, Domonkos I, Farkas T, Wada H, Szalontai B (2002) Low-temperature-induced accumulation of xanthophylls and its structural consequences in the photosynthetic membranes of the cyanobacterium Cylindrospermopsis raciborskii: an FTIR spectroscopic study. P Natl Acad Sci USA 99:2410–2415
Xiang SR, Yao TD, An LZ, Wu GJ, Xu BQ, Ma XJ, Li Z, Wang JX, Yu WS (2005a) Vertical quantitative and dominant population distribution of the bacteria isolated from the Muztagata ice core. Sci China Ser D 48:1728–1739
Xiang SR, Yao TD, An LZ, Xu BL, Wang JX (2005b) 16S rRNA sequences and differences in bacteria isolated from the Muztag Ata glacier at increasing depths. Appl Environ Microbiol 71:4619–4627
Xiang SR, Shang TC, Chen Y, Jing ZF, Yao TD (2009) Changes in diversity and biomass of bacteria along a shallow snow pit from Kuytun 51 Glacier, Tianshan Mountains, China. J Geophys Res Biogeosci 114:380
Xie J, Wang NL, Pu JC, Chen L (2009) Study of the bacterial diversity recovered from glacial snow of the northern Tibetan Plateau (in Chinese). J Glaciol Geocryol 31:342–349
Yao TD, Liu YQ, Kang SC, Jiao NZ, Zeng YH, Liu XB, Zhang YJ (2008) Bacteria variabilities in a Tibetan ice core and their relations with climate change. Glob Biogeochem Cycles 22:285–295
Zhang XJ, Yao TD, Ma XJ, Wang NL (2001) Malan ice core: analyse of microorganism from a deep ice core (in Chinese). Sci China Ser D 31:296–299
Zhang XF, Yao TD, Tian LD, Xu SJ, An LZ (2008) Phylogenetic and physiological diversity of bacteria isolated from Puruogangri ice core. Microb Ecol 55:476–488
Zhang SH, Hou SG, Yang GL, Wang JH (2010) Bacterial community in the East Rongbuk Glacier, Mt. Qomolangma (Everest) by culture and culture-independent methods. Microbiol Res 165:336–345
Acknowledgements
This study was financially supported by the National Natural Science Foundation of China (Grant nos. 41701085, 41425004 and 41371084) and China Postdoctoral Science Foundation (Grant no. 2016M590140). Professor John Hodgkiss of The University of Hong Kong is thanked for his help with our English.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by A. Oren.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Shen, L., Liu, Y., Wang, N. et al. Variation with depth of the abundance, diversity and pigmentation of culturable bacteria in a deep ice core from the Yuzhufeng Glacier, Tibetan Plateau. Extremophiles 22, 29–38 (2018). https://doi.org/10.1007/s00792-017-0973-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00792-017-0973-8