Extremophiles DOI 10.1007/s00792-015-0749-y
REVIEW
The microbial diversity, distribution, and ecology of permafrost in China: a review Weigang Hu1 · Qi Zhang1 · Tian Tian1 · Guodong Cheng2 · Lizhe An1 · Huyuan Feng1
Received: 11 November 2014 / Accepted: 4 April 2015 © Springer Japan 2015
Abstract Permafrost in China mainly located in highaltitude areas. It represents a unique and suitable ecological niche that can be colonized by abundant microbes. Permafrost microbial community varies across geographically separated locations in China, and some lineages are novel and possible endemic. Besides, Chinese permafrost is a reservoir of functional microbial groups involved in key biogeochemical cycling processes. In future, more work is necessary to determine if these phylogenetic groups detected by DNA-based methods are part of the viable microbial community, and their functional roles and how they potentially respond to climate change. This review summaries recent studies describing microbial biodiversity found in permafrost and associated environments in China, and provides a framework for better understanding the microbial ecology of permafrost. Keywords Permafrost · China · Microbial ecology · Biodiversity · Climate change · Qinghai-Tibet Plateau
Communicated by S. Albers. Electronic supplementary material The online version of this article (doi:10.1007/s00792-015-0749-y) contains supplementary material, which is available to authorized users. * Huyuan Feng [email protected] 1
Ministry of Education Key Laboratory of Cell Activities and Stress Adaptations, School of Life Sciences, Lanzhou University, Lanzhou 730000, China
2
State Key Laboratory of Frozen Soil Engineering, Cold and Arid Regions Environmental and Engineer Research Institute, Chinese Academy of Sciences, Lanzhou 730000, China
Introduction An estimated 25 % of Earth’s terrestrial surface is underlain by permafrost. The classic definition of permafrost is ground that remains at or below 0 °C continuously for at least 2 years (Jansson and Tas¸ 2014). The areal extent of permafrost in China ranks third in world after Russia and Canada, and elevationally controlled permafrost, which is called altitudinal or high-altitude permafrost, ranks first (Ran et al. 2012). High-altitude permafrost mainly distribute in mountainous west China, such as the Chinese Altai Mountains, the Chinese Tianshan Mountains, the Qilian Mountains, and the Qinghai-Tibet Plateau (Zhao et al. 2014). A latest map of frozen ground in China, including both permafrost and seasonally frozen ground, shows that the total area of permafrost is estimated at ~1.59 × 106 km2 (Ran et al. 2012; Fig. S1). The extreme characteristics of permafrost lead to early conclusion that permafrost soils were completely devoid of biological entities (Gilichinsky 2002). However, current evidence reveals that many microorganisms are able to adapt and even active at subzero temperatures in permafrost as “a community of survivors” (Friedmann 1994). The microbial ecology of permafrost has recently become the focus of intense research efforts owing to the emerging concerns about the impacts of climate change and possibly subsequent permafrost thaw on the microbial degradation of trapped organic matter, with the increased potential for the release of the greenhouse gases as a consequence (Mackelprang et al. 2011; Jansson and Tas¸ 2014). Compared with latitudinal permafrost in polar regions, altitudinal permafrost, especially permafrost on the Qinghai-Tibet Plateau, is more sensitive to the combined influence of climatic warming and surface conditions (Jin et al. 2000). Recent investigations indicated that most permafrost
13
Extremophiles
regions of China were being affected by climatic warming and significant permafrost degradation had occurred (Li et al. 2008b). Description of abundance, activity, diversity, and distribution of microorganisms in permafrost is crucial to our understanding of how microorganisms survive in permafrost, and how they respond to current climate change and subsequent permafrost thawing. In fact, microbes in permafrost in China have been the subject of meticulous studies over the last decade (Table 1). Microbiologists focus on assembling an inventory, which would cover the taxonomic diversity of microorganisms inhabiting permafrost of various locations in China. In this review, we summarize our current knowledge of the microbial ecology and biodiversity of permafrost in China. To make the picture complete, information on microorganisms from the overlying active layer soils, seasonally frozen ground, and soils affected by discontinuous permafrost is also included.
Microbial abundance of permafrost in China A large number (up to 1010 cells g−1) of microbial cells was detected in permafrost in China but varied over a large range among different permafrost environments (Table 1). Microbial direct counts as determined by epifluorescence microscopy with 4′,6-diamino-2-phenylindole (DAPI) staining ranged from 107 to 109 cells/g of soil or sediment, which were consistent with permafrost samples taken from Arctic, but were relatively higher than Siberian and Antarctic samples (Fig. 1a). Furthermore, the number of aerobic bacterial CFU reached 6 × 107/g of soil or sediment, which was higher than the quantities of Siberian, Arctic, and Antarctic permafrost (Fig. 1b). The variation in the abundance of the microbes in different permafrost environments may reflect the water or nutrient content of the habitat (Shivaji and Reddy 2010 and references therein). In general, only a small percentage of total cells are represented by cultured isolates. For example, in Beilu River (on the Qinghai-Tibet Plateau) permafrost soils, viable cell counts were 102–106 CFU/g of soil, while total counts were in the range of 107–109 cells/g (Feng et al. 2004). Similar results were also found by Wang et al. (2011), Li et al. (2012a), and Zhang et al. (2013b). The lack of cultured organisms might be owing to non-culturable nature of microorganisms (e.g., “dwarf” cells), inappropriate pretreatments of samples (e.g., thawing regimes) or particular microbes requiring specific culture conditions (Steven et al. 2006; Kochkina et al. 2012). On the other hand, direct microbial counts as determined by quantitative PCR or epifluorescence microscopy tend to overestimate total cell counts because dead microbial cells or naked DNA may remain well preserved for long periods of time at constant subzero temperatures in permafrost (Willerslev et al. 2004).
13
Present data show that abundance of microbial community seems to be influenced by specific abiotic factors. For example, with increasing depth or age of permafrost, both the ability to recover viable cells from permafrost and the number of viable and total cells decreased; however, the diversity of bacterial isolates seemed to be independent from permafrost depth (Feng et al. 2004; Zhang et al. 2007a; Wang et al. 2011; Ollivier et al. 2013; Tai et al. 2014). Besides, Zhang et al. (2009) found that archaeal amoA abundance in alpine and permafrost soils significantly decreased with altitude on Mount Everest (Tibet Plateau) and archaeal ammonia oxidizers were more abundant than bacterial ones at altitudes below 5400 m above sea level, while the situation was reversed at higher altitudes. Viable microbial numbers were also different among sampling months (Chen et al. 2011) and vegetation types (Yu and Shi 2011; Li et al. 2012a). Furthermore, microbial abundance was closely correlated with soil physicochemical properties (e.g., soil moisture, pH, organic carbon, and total nitrogen content) (Wang et al. 2011; Zhang et al. 2013b, 2014c; Tai et al. 2014). Therefore, the origin, age, and physiochemical characteristics of permafrost combined with other factors probably determine the abundance of microbial community (also see Steven et al. 2009; Hu et al. 2012).
Diversity of viable microorganisms A considerable diversity of viable microorganisms, including bacteria, archaea, yeasts, filamentous fungi, and microalgae have been detected in permafrost and associated environments in China. A list of microbial generic names recorded as culture from permafrost in China is provided (Table S1). Phylogenetic groups of the bacterial isolates from Chinese permafrost generally fall into six categories: Actinobacteria, Firmicutes, α-Proteobacteria, β-Proteobacteria, γ-Proteobacteria, and Cytophaga-Flavobacterium-Bacteroides (CFB) group (Table S1). This was consistent with previous studies which indicated that these bacterial phyla were also dominant in Arctic permafrost (Steven et al. 2009 and references therein). However, in Antarctic soil samples, a few have been identified to be associated with Deinococcus-Thermus and Spirochaetes except for the aforementioned dominating groups (Shivaji and Reddy 2010). Both Gram-positive and Gram-negative isolates are represented, and spore-forming Bacteria are also commonly isolated, although the abundance of spore-forming Bacteria varies largely among geographically separated permafrost samples. For example, spore-forming genera represented 53 % of culturable bacteria in permafrost samples collected along the Qinghai-Tibet Railway (Liu et al. 2008), but only 18,
4125–4807 4676 NA 4125–4804 NA
Beilu River basin Beilu River basin Beilu River basin Beilu River basin
Haibei
4150–4315 4000–6550
4600
Dongji Cona/Huashixia/Gande
Mount Everest
Wuli Coalfield 4628
3430–3460
Zoige wetland
Beilu River permafrost research station
4300 3430
Qinghai-Tibet Plateau
4779
Kunlun Mountain Pass
Zoige wetland
3573–5231
10 sites between Fenghuoshan and Yangbajin along the Tibetan highway
4301–4546 The source region of the Yangtze River, Yellow River and Lancang River (SRYYL)
20–150
4491
5
NA
0–10
5–90
20–30
10–15
65
50–900
15
0–30
5–20
20–570 10–20 NA 20–570
0–200 NA
4767 5515
Altitude (m) Sampling depth (cm)
Qinghai-Tibet Plateaua Kunlun Mountain Pass The foreland of the Zhadang glacier Tuotuohe
Sampling site
NA
105–106 105–107
0–103
Actinomycetes Bacteria
454 pyrosequencing
qPCR/Clone-sequencing
qPCR/Clone-RFLPsequencing
qPCR/T-RFLP
Anaerobic enrichment cultivation/qPCR/Clonesequencing
Bacteria
NA
NA
Zhang et al. (2013a)
107e/103–104e NA Archaea/AOA
103–108e NA
107–108e/103–104e Peng et al. (2013)
Zhang et al. (2009)
NA
Ollivier et al. (2013) 104–107e
Bacteria/AOB
Ammonia-oxidizing bacteria (AOB) Ammonia-oxidizing archaea (AOA)
NA
NA NA
Methanogenic archaea Bacteria
Zhang et al. (2008a, b)
108–109e NA Archaea
107–109e 105–107e
Tian et al. (2012)
NA
Wei et al. (2014)
Hu et al. (2014)
Li et al. (2008a); Liu, et al. (2008)
Yu and Shi (2011)
Li et al. (2012c), Liu et al. (2014)
Yang et al. (2012a) Zhang et al. (2007a) Feng et al. (2004) Chen et al. (2011) Zhang et al. (2007b)
Liu et al. (2001) Yue et al. (2010)
References
NA
Archaea
NA
NA
103–104
Fungi
NA
NA
105–106
Bacteria
0–10 102–106 107 102–105 NA
T-RFLP/Clone-sequencing Archaea
DGGE/Clone-sequencing
NA NA 107–109 NA NA
105–107 7
NA NA
NAb 104–105
Viable cell countsc Total countsd
NA
Aerobic bacteria Aerobic bacteria Aerobic bacteria Alkaliphilic and psychrotolerant bacteria Oleaginous bacteria/fungi/ yeast/microalgae
Aerobic bacteria
Aerobic bacteria Aerobic bacteria
Cell type
Laboratory cultivation/ Fungi Clone-RFLP-sequencing
Laboratory cultivation/ DGGE
Laboratory cultivation
Laboratory cultivation
Laboratory cultivation Laboratory cultivation Laboratory cultivation Laboratory cultivation
Laboratory cultivation
Laboratory cultivation Laboratory cultivation
Method
Table 1 Summary of studies of microbial biodiversity in permafrost soils in China by culture-dependent and culture-independent methods
Extremophiles
13
13 0–20
0–5
11,000 30–40 30–160 70–160
4520–5100
4718 NA 2905–4130 4053
NA 548 370–480 370–480
19 sites between Xidatan and Liangdaohe along the Tibetan highway Namco
Tibet
Qilian Mountains Binggou Muli coal field
Da and Xiao Xing’an Mountains Mo-he basin
Mo-he country
Walagan/Tayuan/Jiagedaqi
NA 150–300
NA 3833
Data not available
454 pyrosequencing
DGGE-sequencing
Laboratory cultivation
Laboratory cultivation
Laboratory cultivation Laboratory cultivation
454 pyrosequencing
454 pyrosequencing
Clone-sequencing
Laboratory cultivation/ Clone-sequencing
Laboratory cultivation Clone-sequencing
Metagenomic sequencing
Cells per gram of soil or sediment (only the order of magnitude of the counts are presented)
Assessed by real-time PCR quantification
e
d
NA NA
NA
Bacteria
Bacteria/Archaea
Aerobic bacteria/fungi
Aerobic bacteria
Aerobic bacteria Aerobic bacteria
Bacteria
Bacteria
Bacteria
Bacteria
NA NA
NA
NA
107–108 NA
104–105 NA
NA NA
NA
NA
NA
NA
Wu et al. (2012a)
Yang et al. (2008)
Wang et al. (2011) Zhang et al. (2008c)
Bai et al. (2006) Bai et al. (2005)
Yang et al. (2014)
Yang et al. (2012b)
Dan et al. (2014)
Li et al. (2012b)
Tai et al. (2014) Han et al. (2011)
Guan et al. (2013)
108e NA NA NA
Yun et al. (2014)
1010e
105 103
NA
NA
NA
NA
106–107 Bacteria/Fungi/mcrA/pmo NA A/mmoX/mxaF
Aerobic bacteria
Bacteria
Methanotrophic bacteria
qPCR/454 pyrosequencing Bacteria
NA
NA 106–107
Fungi Laboratory cultivation/454 Bacteria pyrosequencing/Biolog EcoPlates
Li et al. (2012a); Zhang et al. (2014c)
Zhang et al. (2013b)
108
105
Laboratory cultivation/454 Bacteria pyrosequencing/Biolog EcoPlates 108–109
References
Cell type
Viable cell countsc Total countsd
Method
CFU per gram of soil or sediment (only the order of magnitude of the counts are presented)
c
b
Sampling locations are indicated in bold
a
0–200
3586
5
100–284 135–150
0–60 14500– 28500
3833 3564/3760
The foreland of the Tianshan No. 1 4486 glacier
The root of Saussurea involucrata Kar.et Kir.etMaxim. The mouth of the ice-free cirque
Tianshan Mountains The mouth of the ice-free cirque The ice-free cirque/The Tianshan No. 1 glacier Daxigou meteorological station
Walagan/Tayuan/Jiagedaqi
0–20
4885
Beilu River permafrost research station
3–20
Altitude (m) Sampling depth (cm)
Sampling site
Table 1 continued
Extremophiles
Extremophiles
Fig. 1 Boxplots of microbial abundance in various permafrost environments. a Total direct counts in permafrost in China (107–109 cells/g), Arctic (107–109; Hansen et al. 2007; Steven et al. 2007, 2008), Siberia (103–108; Gilichinsky 2002; Vishnivetskaya et al. 2006), and Antarctic (103–108; Aislabie et al. 2006; Gilichinsky et al. 2007), respectively. b Viable bacteria counts in permafrost in China (0–107 CFU/g), Arctic (0–106; Hansen et al. 2007; Steven et al. 2007, 2008), Siberia (0–107; Shi et al. 1997; Vishnivetskaya et al. 2000;
Gilichinsky 2002; Vishnivetskaya et al. 2006) and Antarctic (0–105; Vorobyova et al., 1997; Aislabie et al. 2006; Gilichinsky et al. 2007), respectively. Components of the boxplot are: top of the box, upper quartile; midline of box, median; bottom of box, lower quartile; bars, 1.5 times length of box (1.5 times the horizontal spread); dots, values that are > or
REVIEW
The microbial diversity, distribution, and ecology of permafrost in China: a review Weigang Hu1 · Qi Zhang1 · Tian Tian1 · Guodong Cheng2 · Lizhe An1 · Huyuan Feng1
Received: 11 November 2014 / Accepted: 4 April 2015 © Springer Japan 2015
Abstract Permafrost in China mainly located in highaltitude areas. It represents a unique and suitable ecological niche that can be colonized by abundant microbes. Permafrost microbial community varies across geographically separated locations in China, and some lineages are novel and possible endemic. Besides, Chinese permafrost is a reservoir of functional microbial groups involved in key biogeochemical cycling processes. In future, more work is necessary to determine if these phylogenetic groups detected by DNA-based methods are part of the viable microbial community, and their functional roles and how they potentially respond to climate change. This review summaries recent studies describing microbial biodiversity found in permafrost and associated environments in China, and provides a framework for better understanding the microbial ecology of permafrost. Keywords Permafrost · China · Microbial ecology · Biodiversity · Climate change · Qinghai-Tibet Plateau
Communicated by S. Albers. Electronic supplementary material The online version of this article (doi:10.1007/s00792-015-0749-y) contains supplementary material, which is available to authorized users. * Huyuan Feng [email protected] 1
Ministry of Education Key Laboratory of Cell Activities and Stress Adaptations, School of Life Sciences, Lanzhou University, Lanzhou 730000, China
2
State Key Laboratory of Frozen Soil Engineering, Cold and Arid Regions Environmental and Engineer Research Institute, Chinese Academy of Sciences, Lanzhou 730000, China
Introduction An estimated 25 % of Earth’s terrestrial surface is underlain by permafrost. The classic definition of permafrost is ground that remains at or below 0 °C continuously for at least 2 years (Jansson and Tas¸ 2014). The areal extent of permafrost in China ranks third in world after Russia and Canada, and elevationally controlled permafrost, which is called altitudinal or high-altitude permafrost, ranks first (Ran et al. 2012). High-altitude permafrost mainly distribute in mountainous west China, such as the Chinese Altai Mountains, the Chinese Tianshan Mountains, the Qilian Mountains, and the Qinghai-Tibet Plateau (Zhao et al. 2014). A latest map of frozen ground in China, including both permafrost and seasonally frozen ground, shows that the total area of permafrost is estimated at ~1.59 × 106 km2 (Ran et al. 2012; Fig. S1). The extreme characteristics of permafrost lead to early conclusion that permafrost soils were completely devoid of biological entities (Gilichinsky 2002). However, current evidence reveals that many microorganisms are able to adapt and even active at subzero temperatures in permafrost as “a community of survivors” (Friedmann 1994). The microbial ecology of permafrost has recently become the focus of intense research efforts owing to the emerging concerns about the impacts of climate change and possibly subsequent permafrost thaw on the microbial degradation of trapped organic matter, with the increased potential for the release of the greenhouse gases as a consequence (Mackelprang et al. 2011; Jansson and Tas¸ 2014). Compared with latitudinal permafrost in polar regions, altitudinal permafrost, especially permafrost on the Qinghai-Tibet Plateau, is more sensitive to the combined influence of climatic warming and surface conditions (Jin et al. 2000). Recent investigations indicated that most permafrost
13
Extremophiles
regions of China were being affected by climatic warming and significant permafrost degradation had occurred (Li et al. 2008b). Description of abundance, activity, diversity, and distribution of microorganisms in permafrost is crucial to our understanding of how microorganisms survive in permafrost, and how they respond to current climate change and subsequent permafrost thawing. In fact, microbes in permafrost in China have been the subject of meticulous studies over the last decade (Table 1). Microbiologists focus on assembling an inventory, which would cover the taxonomic diversity of microorganisms inhabiting permafrost of various locations in China. In this review, we summarize our current knowledge of the microbial ecology and biodiversity of permafrost in China. To make the picture complete, information on microorganisms from the overlying active layer soils, seasonally frozen ground, and soils affected by discontinuous permafrost is also included.
Microbial abundance of permafrost in China A large number (up to 1010 cells g−1) of microbial cells was detected in permafrost in China but varied over a large range among different permafrost environments (Table 1). Microbial direct counts as determined by epifluorescence microscopy with 4′,6-diamino-2-phenylindole (DAPI) staining ranged from 107 to 109 cells/g of soil or sediment, which were consistent with permafrost samples taken from Arctic, but were relatively higher than Siberian and Antarctic samples (Fig. 1a). Furthermore, the number of aerobic bacterial CFU reached 6 × 107/g of soil or sediment, which was higher than the quantities of Siberian, Arctic, and Antarctic permafrost (Fig. 1b). The variation in the abundance of the microbes in different permafrost environments may reflect the water or nutrient content of the habitat (Shivaji and Reddy 2010 and references therein). In general, only a small percentage of total cells are represented by cultured isolates. For example, in Beilu River (on the Qinghai-Tibet Plateau) permafrost soils, viable cell counts were 102–106 CFU/g of soil, while total counts were in the range of 107–109 cells/g (Feng et al. 2004). Similar results were also found by Wang et al. (2011), Li et al. (2012a), and Zhang et al. (2013b). The lack of cultured organisms might be owing to non-culturable nature of microorganisms (e.g., “dwarf” cells), inappropriate pretreatments of samples (e.g., thawing regimes) or particular microbes requiring specific culture conditions (Steven et al. 2006; Kochkina et al. 2012). On the other hand, direct microbial counts as determined by quantitative PCR or epifluorescence microscopy tend to overestimate total cell counts because dead microbial cells or naked DNA may remain well preserved for long periods of time at constant subzero temperatures in permafrost (Willerslev et al. 2004).
13
Present data show that abundance of microbial community seems to be influenced by specific abiotic factors. For example, with increasing depth or age of permafrost, both the ability to recover viable cells from permafrost and the number of viable and total cells decreased; however, the diversity of bacterial isolates seemed to be independent from permafrost depth (Feng et al. 2004; Zhang et al. 2007a; Wang et al. 2011; Ollivier et al. 2013; Tai et al. 2014). Besides, Zhang et al. (2009) found that archaeal amoA abundance in alpine and permafrost soils significantly decreased with altitude on Mount Everest (Tibet Plateau) and archaeal ammonia oxidizers were more abundant than bacterial ones at altitudes below 5400 m above sea level, while the situation was reversed at higher altitudes. Viable microbial numbers were also different among sampling months (Chen et al. 2011) and vegetation types (Yu and Shi 2011; Li et al. 2012a). Furthermore, microbial abundance was closely correlated with soil physicochemical properties (e.g., soil moisture, pH, organic carbon, and total nitrogen content) (Wang et al. 2011; Zhang et al. 2013b, 2014c; Tai et al. 2014). Therefore, the origin, age, and physiochemical characteristics of permafrost combined with other factors probably determine the abundance of microbial community (also see Steven et al. 2009; Hu et al. 2012).
Diversity of viable microorganisms A considerable diversity of viable microorganisms, including bacteria, archaea, yeasts, filamentous fungi, and microalgae have been detected in permafrost and associated environments in China. A list of microbial generic names recorded as culture from permafrost in China is provided (Table S1). Phylogenetic groups of the bacterial isolates from Chinese permafrost generally fall into six categories: Actinobacteria, Firmicutes, α-Proteobacteria, β-Proteobacteria, γ-Proteobacteria, and Cytophaga-Flavobacterium-Bacteroides (CFB) group (Table S1). This was consistent with previous studies which indicated that these bacterial phyla were also dominant in Arctic permafrost (Steven et al. 2009 and references therein). However, in Antarctic soil samples, a few have been identified to be associated with Deinococcus-Thermus and Spirochaetes except for the aforementioned dominating groups (Shivaji and Reddy 2010). Both Gram-positive and Gram-negative isolates are represented, and spore-forming Bacteria are also commonly isolated, although the abundance of spore-forming Bacteria varies largely among geographically separated permafrost samples. For example, spore-forming genera represented 53 % of culturable bacteria in permafrost samples collected along the Qinghai-Tibet Railway (Liu et al. 2008), but only 18,
4125–4807 4676 NA 4125–4804 NA
Beilu River basin Beilu River basin Beilu River basin Beilu River basin
Haibei
4150–4315 4000–6550
4600
Dongji Cona/Huashixia/Gande
Mount Everest
Wuli Coalfield 4628
3430–3460
Zoige wetland
Beilu River permafrost research station
4300 3430
Qinghai-Tibet Plateau
4779
Kunlun Mountain Pass
Zoige wetland
3573–5231
10 sites between Fenghuoshan and Yangbajin along the Tibetan highway
4301–4546 The source region of the Yangtze River, Yellow River and Lancang River (SRYYL)
20–150
4491
5
NA
0–10
5–90
20–30
10–15
65
50–900
15
0–30
5–20
20–570 10–20 NA 20–570
0–200 NA
4767 5515
Altitude (m) Sampling depth (cm)
Qinghai-Tibet Plateaua Kunlun Mountain Pass The foreland of the Zhadang glacier Tuotuohe
Sampling site
NA
105–106 105–107
0–103
Actinomycetes Bacteria
454 pyrosequencing
qPCR/Clone-sequencing
qPCR/Clone-RFLPsequencing
qPCR/T-RFLP
Anaerobic enrichment cultivation/qPCR/Clonesequencing
Bacteria
NA
NA
Zhang et al. (2013a)
107e/103–104e NA Archaea/AOA
103–108e NA
107–108e/103–104e Peng et al. (2013)
Zhang et al. (2009)
NA
Ollivier et al. (2013) 104–107e
Bacteria/AOB
Ammonia-oxidizing bacteria (AOB) Ammonia-oxidizing archaea (AOA)
NA
NA NA
Methanogenic archaea Bacteria
Zhang et al. (2008a, b)
108–109e NA Archaea
107–109e 105–107e
Tian et al. (2012)
NA
Wei et al. (2014)
Hu et al. (2014)
Li et al. (2008a); Liu, et al. (2008)
Yu and Shi (2011)
Li et al. (2012c), Liu et al. (2014)
Yang et al. (2012a) Zhang et al. (2007a) Feng et al. (2004) Chen et al. (2011) Zhang et al. (2007b)
Liu et al. (2001) Yue et al. (2010)
References
NA
Archaea
NA
NA
103–104
Fungi
NA
NA
105–106
Bacteria
0–10 102–106 107 102–105 NA
T-RFLP/Clone-sequencing Archaea
DGGE/Clone-sequencing
NA NA 107–109 NA NA
105–107 7
NA NA
NAb 104–105
Viable cell countsc Total countsd
NA
Aerobic bacteria Aerobic bacteria Aerobic bacteria Alkaliphilic and psychrotolerant bacteria Oleaginous bacteria/fungi/ yeast/microalgae
Aerobic bacteria
Aerobic bacteria Aerobic bacteria
Cell type
Laboratory cultivation/ Fungi Clone-RFLP-sequencing
Laboratory cultivation/ DGGE
Laboratory cultivation
Laboratory cultivation
Laboratory cultivation Laboratory cultivation Laboratory cultivation Laboratory cultivation
Laboratory cultivation
Laboratory cultivation Laboratory cultivation
Method
Table 1 Summary of studies of microbial biodiversity in permafrost soils in China by culture-dependent and culture-independent methods
Extremophiles
13
13 0–20
0–5
11,000 30–40 30–160 70–160
4520–5100
4718 NA 2905–4130 4053
NA 548 370–480 370–480
19 sites between Xidatan and Liangdaohe along the Tibetan highway Namco
Tibet
Qilian Mountains Binggou Muli coal field
Da and Xiao Xing’an Mountains Mo-he basin
Mo-he country
Walagan/Tayuan/Jiagedaqi
NA 150–300
NA 3833
Data not available
454 pyrosequencing
DGGE-sequencing
Laboratory cultivation
Laboratory cultivation
Laboratory cultivation Laboratory cultivation
454 pyrosequencing
454 pyrosequencing
Clone-sequencing
Laboratory cultivation/ Clone-sequencing
Laboratory cultivation Clone-sequencing
Metagenomic sequencing
Cells per gram of soil or sediment (only the order of magnitude of the counts are presented)
Assessed by real-time PCR quantification
e
d
NA NA
NA
Bacteria
Bacteria/Archaea
Aerobic bacteria/fungi
Aerobic bacteria
Aerobic bacteria Aerobic bacteria
Bacteria
Bacteria
Bacteria
Bacteria
NA NA
NA
NA
107–108 NA
104–105 NA
NA NA
NA
NA
NA
NA
Wu et al. (2012a)
Yang et al. (2008)
Wang et al. (2011) Zhang et al. (2008c)
Bai et al. (2006) Bai et al. (2005)
Yang et al. (2014)
Yang et al. (2012b)
Dan et al. (2014)
Li et al. (2012b)
Tai et al. (2014) Han et al. (2011)
Guan et al. (2013)
108e NA NA NA
Yun et al. (2014)
1010e
105 103
NA
NA
NA
NA
106–107 Bacteria/Fungi/mcrA/pmo NA A/mmoX/mxaF
Aerobic bacteria
Bacteria
Methanotrophic bacteria
qPCR/454 pyrosequencing Bacteria
NA
NA 106–107
Fungi Laboratory cultivation/454 Bacteria pyrosequencing/Biolog EcoPlates
Li et al. (2012a); Zhang et al. (2014c)
Zhang et al. (2013b)
108
105
Laboratory cultivation/454 Bacteria pyrosequencing/Biolog EcoPlates 108–109
References
Cell type
Viable cell countsc Total countsd
Method
CFU per gram of soil or sediment (only the order of magnitude of the counts are presented)
c
b
Sampling locations are indicated in bold
a
0–200
3586
5
100–284 135–150
0–60 14500– 28500
3833 3564/3760
The foreland of the Tianshan No. 1 4486 glacier
The root of Saussurea involucrata Kar.et Kir.etMaxim. The mouth of the ice-free cirque
Tianshan Mountains The mouth of the ice-free cirque The ice-free cirque/The Tianshan No. 1 glacier Daxigou meteorological station
Walagan/Tayuan/Jiagedaqi
0–20
4885
Beilu River permafrost research station
3–20
Altitude (m) Sampling depth (cm)
Sampling site
Table 1 continued
Extremophiles
Extremophiles
Fig. 1 Boxplots of microbial abundance in various permafrost environments. a Total direct counts in permafrost in China (107–109 cells/g), Arctic (107–109; Hansen et al. 2007; Steven et al. 2007, 2008), Siberia (103–108; Gilichinsky 2002; Vishnivetskaya et al. 2006), and Antarctic (103–108; Aislabie et al. 2006; Gilichinsky et al. 2007), respectively. b Viable bacteria counts in permafrost in China (0–107 CFU/g), Arctic (0–106; Hansen et al. 2007; Steven et al. 2007, 2008), Siberia (0–107; Shi et al. 1997; Vishnivetskaya et al. 2000;
Gilichinsky 2002; Vishnivetskaya et al. 2006) and Antarctic (0–105; Vorobyova et al., 1997; Aislabie et al. 2006; Gilichinsky et al. 2007), respectively. Components of the boxplot are: top of the box, upper quartile; midline of box, median; bottom of box, lower quartile; bars, 1.5 times length of box (1.5 times the horizontal spread); dots, values that are > or
