Niche Specificity and Potential Functions of Microbial Communities in Karst Caves as Exampled by Panlong Cave in Guilin City, Guangxi
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摘要: 开展岩溶洞穴不同生境微生物与环境因子间的研究，对阐明深部生物圈微生物的多样性、潜在功能及环境驱动机制具有重要意义.以广西桂林盘龙洞为例，通过对细菌16S rRNA高通量测序系统研究了洞穴7种小生境细菌群落的空间分布特征及其与环境因子之间的关系.研究发现温度是驱动盘龙洞细菌群落组成的重要因素，微生物群落组成及潜在生态功能均具有生境特异性，不同生境具有独有的细菌指示类群.滴水、干燥石笋表面生物膜、湿润石笋表面生物膜3个生境与洞穴氮循环密切相关，风化结皮、沉积物、岩壁3个生境与洞穴微生物固定二氧化碳关系紧密.此外，洞穴细菌通过密切的代谢交换形成协作的正相关关系，暗示着微生物在洞穴这一极端环境中的生存策略.Abstract: Karst caves serve as the natural laboratories to study subsurface biosphere, which provide ideal places to investigate microbial diversity and their interactions between microbes and environments. Guilin is one of the typical areas with developed karst landscape. Deep investigation of cave microbes in different niches and their response to environmental variables will provide valuable information on subsurface biosphere in terms of microbial diversity, function and interaction with environments. To this end, Samples were collected from overlying soils, sediments, cave wall, weathered crusted on cave walls, microbial biofilm on stalagmite surface and dripping water in the Panlong Cave in Guiling City to study microbial communities and their correlation with environmental variables via high throughput sequencing of 16S rRNA. Results show that bacterial communities show high specificity to niches and were dominated by Actinomycete and Proteobacteria. Each niche has its own specific indicator group. For example, Paemibacillus was the indicator for microbial biofilm on the dry surface of stalagmite, whilst Acidobacteriaceae and Pseudomonas were the indicator groups in microbial biofilm on the wet surface of stalagmite. Pseudomonadales and Branhamella were the indicator groups in dripping water, whereas indicator groups in overlying soils included Mycobacterium and Nocardioides. Bacillus and Gp-7 were indicators in sediments, whilst Chromatiales, Soilrubrobacteraceae and Rubrobcter were indicators in cave wall and Methylobacterium in weathered crust. Temperature was demonstrated to be the main variable impacting bacterial communities in the Panlong Cave as indicated by redundancy analysis. Tax4fun2 analysis shows that microbes participated in carbon and nitrogen cycles also varied with niches. Microbes in dripping water, microbial biofilm on dry/wet surface of stalagmite were closely related to nitrogen cycle. On the contrast, those in weathered crust, sediments and cave wall were more involved in carbon fixation. Co-occurrence network analysis inferred that corporation was the main strategy for microbial groups to survive in the oligotrophic karst caves.
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Key words:
- karst cave /
- subsurface biosphere /
- carbon fixation /
- nitrogen cycle /
- co-occurrence network /
- geomicrobiology
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图 1 广西桂林盘龙洞采样点分布示意图(a)以及采样点的照片(b~h)
b.上覆土壤（OS）；c.7号点岩壁（W）与风化结皮（WC）；d.10号点岩壁与风化结皮；e.7号点干燥石笋（DS）；f.7号点湿润石笋（WS）；g.8号点干燥石笋；h.9号点湿润石笋
Fig. 1. Schematic diagram of sampling sites in the Panlong Cave, Guilin City, Guangxi (a) and images of sampling sites in situ (b-h)
图 2 桂林盘龙洞微生物群落结构及不同生境中微生物群落的指示类群
a.相对丰度前10的门的组成；b.相对丰度前15的属组成；c.基于LEfSe分析确定的不同生境的指示类群（LDA SCORE > 4）；d.基于ASVs水平的微生物群落非度量多维尺度分析（NMDS）；DW.滴水；S.沉积物；WC.风化结皮；W.岩壁；DS.干石笋表面生物膜；OS.上覆土壤；WS.湿石笋表面生物膜
Fig. 2. Microbial community compositions and microbial indicator groups of different niches in the Panlong Cave, Guilin City
图 3 广西桂林盘龙洞中细菌群落结构与环境因子之间的冗余分析(RDA)(a)及不同微生物类群与环境因子的相关性热图(b)
图中*和**分别代表P<0.05和P<0.01
Fig. 3. Redundancy analysis (RDA) (a) and the heatmap (b) of microbial communities and environmental parameters in the Panlong Cave, Guilin City, Guangxi
图 4 基于Tax4fun2数据库对盘龙洞细菌群落参与洞穴元素循环功能预测图; (a)氮循环; (b)碳固定
图中数字代表该生境中的酶在此元素循环通路中丰度的排名，灰色方块代表未在此生境中检测到与该元素循环相关的酶
Fig. 4. Function predictions related to nitrogen (a) and carbon (b) cycles based on 16S rRNA against Tax4fun2 database in the Panlong Cave, Guangxi
图 5 盘龙洞细菌群落的共现网络分析.(a)按模块着色；(b)按门类着色；(c)来自不同生境的节点在网络模块中所占比例
每个节点的大小与其连接数量成正比，其中粉色代表正相关，绿色代表负相关.S、W、OS、WC、DW、WS、DS分别代表沉积物，岩壁，上覆土壤，风化结皮，滴水，湿石笋表面生物膜，干石笋表面生物膜
Fig. 5. The co-occurrence network analysis of bacterial communities colored by taxonomy (a) and by modules (b) in the Panlong Cave, Guilin City, Guangxi. The node size is proportional to the number of connections. Positive links were in pink and negative ones in green. (c) Relative abundance of bacterial ASVs within individual modules in the networks
表 1 广西桂林盘龙洞洞穴中各个生境样本α多样性指数
Table 1. α diversity index of microbial communities in various habitats in the Panlong Cave, Guilin City, Guangxi
生境 Simpson Chao1 ACE Shannon S 0.98±0.02a 1 449.64±218.07bc 1 454.32±218.59bc 8.13±0.67ab W 0.98±0.03a 1 372.14±397.49bc 1 374.13±402.37bcd 8.12±0.91ab OS 0.98±0.03a 2 244.26±562.91a 2 224.21±553.77a 8.95±1.12a WC 0.98±0.01a 1 053.27±377.47cd 1 058.01±373.47cd 7.67±0.95b DW 0.86±0.01b 965.02±361.88d 982.32±377.49d 5.6±0.45c WS 0.98±0.03a 1 517.85±145.02b 1 519.34±139.96b 8.29±0.79ab DS 0.99±0.00a 1 667.17±331.51b 1 662.63±335.29b 8.97±0.27a 注：不同字母(a~d)表示生境中存在显著性差异(P<0.05)；S.沉积物，W.岩壁，OS.上覆土壤，WC.风化结皮，DW.滴水，WS.湿石笋表面生物膜，DS.干石笋表面生物膜. 
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表 2 广西桂林盘龙洞内各样品的理化参数
Table 2. Physicochemical parameters of samples in the Panlong Cave in Guilin City, Guangxi
样品名 Cl-
(mg/kg)SO42-
(mg/kg)K+
(mg/kg)Na+
(mg/kg)Si4+
(mg/kg)Ca/Mg pH TOC（%） C/N 温度（℃） PLD1W 2.04±0.13 108.72±12.57 8.64±0.11 7.14±1.85 15.36±0.50 8.21±0.05 9.14±0.03 2.68 82.76 10.80 PLD1S 1.32±0.08 35.70±0.42 1.98±0.04 8.10±9.62 5.94±7.51 7.47±0.10 8.44±0.04 1.82 11.49 10.80 PLD2W 2.16±0.11 296.82±2.03 52.50±1.88 6.84±0.44 37.92±5.57 4.08±2.12 8.39±0.03 0.73 5.64 13.60 PLD2S 0.66±0.14 20.34±0.27 0.78±0.06 6.36±0.70 16.56±2.13 18.9±0.70 8.39±0.01 1.45 7.66 13.60 PLD3W 3.36±0.62 30.66±9.12 6.54±0.13 12.72±7.02 51.78±5.63 5.06±0.09 9.04±0.01 1.57 122.95 17.10 PLD3S 10.98±0.11 134.52±1.97 22.44±0.91 6.96±0.71 14.52±1.24 2.10±0.02 8.41±0.04 0.77 7.21 17.10 PLD4W 2.34±0.14 61.92±0.49 4.44±0.07 7.74±0.92 17.58±1.86 8.10±0.06 8.95±0.02 2.79 246.82 16.40 PLD4S 24.66±0.94 606.84±20.39 42.06±0.95 8.34±9.34 6.06±7.34 4.50±0.03 7.80±0.01 0.58 6.00 16.40 PLD5W 6.24±0.08 97.68±9.17 5.58±0.47 8.46±0.46 17.88±2.39 22.13±0.48 8.41±0.04 2.93 50.65 17.40 PLD5S 23.64±0.17 1 682.04±77.99 148.62±3.90 8.28±0.77 19.32±1.70 8.18±0.01 7.83±0.04 0.38 5.32 17.40 PLD6W 2.04±0.07 40.68±0.23 5.34±0.06 9.72±2.06 27.84±8.95 30.63±0.57 8.73±0.02 3.67 63.71 17.90 PLD6S 10.32±1.21 1 374.60±18.00 36.00±1.30 6.48±0.42 14.64±3.97 14.29±0.13 8.15±0.03 0.54 5.37 17.90 PLD7W 2.82±0.09 26.04±0.31 6.06±6.07 8.10±2.05 21.60±15.73 3.54±0.35 9.19±0.03 5.48 302.34 18.30 PLD7S 8.70±0.04 63.84±1.52 12.72±0.37 10.02±1.93 33.66±14.77 6.41±0.14 8.62±0.02 4.46 172.81 18.30 PLD8W 3.24±0.00 18.18±0.90 29.52±23.06 10.68±6.12 19.20±7.74 3.63±0.71 9.05±0.07 1.81 201.72 18.60 PLD8S 1.62±0.07 14.46±0.34 222.54±88.59 15.48±4.98 28.50±4.40 0.94±0.45 8.46±0.03 3.71 146.12 18.60 PLD9W 3.36±0.00 21.54±0.37 1.38±0.04 10.68±4.85 21.42±6.90 31.29±12.42 8.73±0.01 2.77 147.06 18.70 PLD9S 6.18±0.07 68.10±0.20 72.84±83.33 15.06±4.36 28.98±5.75 17.81±10.48 8.14±0.02 5.76 156.64 18.70 PLD10W 5.22±0.01 68.82±0.20 0.84±0.29 8.52±1.25 22.68±2.85 26.42±1.83 9.26±0.04 4.08 353.98 19.30 PLD10S 0.54±0.02 34.98±24.30 32.52±0.85 9.42±1.74 22.50±8.22 8.07±0.2 8.57±0.03 0.28 4.02 19.30
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