云南亚福莱特拟地花菌菌塘土壤微生物群落组成

Composition of shiroes soil microbial community of Albatrellopsis flettioides in Yunnan Province, southwest China

ZHOU Hongmin ,1,#, CHEN Jian ,1,#, LIU Honggao ,2, ZHOU Meng , ,1,*

1 Institute of Microbiology, School of Ecology and Nature Conservation, Beijing Forestry University, Beijing 100083, China

2 Yunnan Key Laboratory of Gastrodia and Fungi Symbiotic Biology, Zhaotong University, Zhaotong 657000, Yunnan, China

亚福莱特拟地花菌Albatrellopsis flettioides J. Kahn隶属于担子菌门Basidiomycota，伞菌纲Agaricomycetes，红菇目Russulales，地花菌科Albatrellaceae，广义地花菌属Albatrellus s.l. (Audet 2010)。广义地花菌属真菌广泛分布在北温带的森林中(Ginns 1997；Dai 2012；Ryvarden & Melo 2017)，在我国主要分布在云南省、四川省及西藏自治区等地(Zheng & Liu 2008)。

亚福莱特拟地花菌俗称黄虎掌，常见于云南中部到北部菌物市场，其菌体肥厚、味道鲜美，是当地人们广泛接受和喜爱的菌根食用菌(Wu et al. 2019)。广义地花菌属真菌与大多数的森林大型真菌一样，其研究多聚焦于地上部分具有子实体的物种多样性(Wu et al. 2016；Chen et al. 2021；Wang et al. 2021；Yuan et al. 2021；Yuan et al. 2022)，以及地花子实体的提取物(Boudagga et al. 2022；Chen et al. 2022)。根据Index Fungorum上的记录，目前地花菌属共有43条记录，其中多数是外生菌根菌，与多种松科植物形成共生关系，如冷杉属Abies、云杉属Picea及松属Pinus (Ginns 1997；Zheng & Liu 2008)。有研究表明，广义地花菌有很高的药用价值，从中提取出的化合物具有抗氧化活性、抗肿瘤、抑制细菌和降低胆固醇的作用(Kawagishi et al. 1996；Nukata et al. 2002；Hashimoto et al. 2005；刘明华等 2005；李正鹏等 2014；Wu et al. 2019)。

随着DNA高通量测序技术的发展，人们对土壤微生物群落多样性进行了广泛而细致的研究(Falkowski et al. 2008；朱永官等 2017；张从明等 2023)。大型菌根食用菌的地下菌丝、宿主根系及周围的腐质土壤结合形成的团状结构通常称为菌塘，关于菌塘土壤微生物组成的报道还很少。研究表明，寄主植物年龄和土壤微生物群落的组成是影响牛肝菌菌丝生长频率和菌丝量的重要生物因素(Santolamazza-Carbone et al. 2023)。部分学者对华丽牛肝菌Boletus magnificus W.F. Chiu、西藏黄绿卷毛菇Floccularia luteovirens (Alb. & Schwein.) Pouzar，以及3种块菌黑孢块菌Tuber melanosporum Vittad.、意大利白块菌T. magnatum Picco及印度块菌T. indicum Cooke & Massee菌塘土壤微生物群落组成进行了探究(邓晓娟等 2018；伍燕等 2021；徐钡昌等 2022)，但对于亚福莱特拟地花菌菌塘土壤微生物群落组成的相关研究还未见报道。

本试验样品采自云南省剑川县印盒山云南松Pinus yunnanensis混交林中，选取亚福莱特拟地花菌的菌塘土壤以及同样立地条件非菌塘土壤进行高通量测序。对亚福莱特拟地花菌菌塘土壤生物群落进行了研究，探讨影响地花菌子实体形成的微生物因素。

1 材料与方法

1.1 研究区概况

试验土壤采自云南省大理白族自治州剑川县，该地区处于三江并流的南端，有矿藏丰富的矿带。年平均气温13.1 ℃，年均降雨量572.7 mm，属于高原季风气候，冬季长但不寒冷，夏季短暂但无酷暑，年温差小、日温差大。采样地点为印盒山26.39°-26.44°N；99.90°-99.92°E，位于黑惠江合江处东侧。云南松、高山栎和杜鹃是该地优势树种。

1.2 样品采集

土壤采集：在2022年8月进行土壤样品采集工作，通过前期大面积踏查选定采集地。菌塘组(a)：选取亚福莱特拟地花菌生长直径范围20 cm，深20 cm的土壤(王淼等 2014)，去掉表面枯枝落叶层，采用五点取样法，混匀，用2 mm的土筛过筛后，装入灭菌后的离心管，放在随身携带的装有干冰的保温箱里保存。非菌塘组(b)：选取5 m外的无亚福莱特拟地花菌生长的土壤。地花样品做好标记，留存备用。重复选取有亚福莱特拟地花菌生长的点取土样以及其相应的非菌塘土壤各10组。

1.3 DNA提取和PCR扩增

样品全程低温运送至上海派森诺生物科技股份有限公司，选用CTAB法参照满孝武等(2022)的步骤进行DNA提取与高通量测序，用Nanodrop对DNA进行定量，并用1.2%的琼脂糖凝胶检测DNA提取质量。真菌ITS区基因扩增引物为ITS5-F (5ʹ-GGAAGTAAAAGTCGTAAC AAGG-3ʹ)和ITS2-R (5ʹ-GCTGCGTTCTTCATCGA TGC-3ʹ)。细菌16S区基因扩增引物为799-F (5ʹ-AACMGGATTAGATACCCKG-3ʹ)和1193-R (5ʹ-ACGTCATCCCCACCTTCC-3ʹ)。使用Agilent Bioanalyzer对文库进行质检，并且通过Quant-iT PicoGreen dsDNA Assay Kit检测文库浓度(大于2 nmol/L)。DNA文库混合后，用MiSeq (Illumina)仪器进行双端测序。

1.4 序列处理和生物信息分析

对原始序列进行质量初筛后，按照index和barcode信息，进行文库和样本划分，并去除barcode序列。用Rstudio软件(Liu et al. 2020)进行双端序列拼接、引物切除，去除冗余设置使用序列的最小出现频次为8，再用Usearch的Unoise3模块去噪与聚类分析，获得特征序列(amplicon sequence variants, ASVs)，去除质体与非细菌。借助数据库unite_all_2021.5.10.fa和silva_16s_v123.fa进行注释。最后等量抽样标准化。

2 结果与分析

2.1 多样性分析

本试验一共获得的真菌和细菌序列分别为1 336 725和762 154条，使用Vsearch (Rognes et al. 2016)对拼接序列进行质控，获得有效序列992 392和690 891条，序列长度集中在200- 300 bp和400-435 bp。借助数据库Unite_all_ 2021.5.10.fa和Silva_16s_v123.fa分别对真菌和细菌进行注释，最终得到1 263条真菌和6 502条细菌扩增子系列变异特征序列(amplicon sequence variants, ASVs)。

对于菌塘组和非菌塘组进行α多样性分析表明，菌塘组真菌的Richness、Chao1、Simpson和Shannon多样性指数差异不明显；其中菌塘组真菌的Richness、Chao1指数显著大于非菌塘组(P<0.01) (图1)。

图1

图1  亚福莱特拟地花菌菌塘(a)以及周围非菌塘(b)土壤样品的真菌(A-D)和细菌(E-H)群落的α多样性

Fig. 1  Alpha diversity of fungi (A-D) and bacteria (E-H) in shiroes (a) soil of Albatrellus flettioides and non-shiroes (b).

对菌塘组和非菌塘组的土壤真菌和细菌的组成差异进行分析。结果显示，地花菌菌塘与非菌塘土壤样品相互分离，即菌塘组与非菌塘组的真菌和细菌群落结构存在差异。其中PCo 1解释了20.63%的真菌和28.81%的细菌的差异性。PCo 2解释了15.11%的真菌和14.95%的细菌差异性(图2)。

图2

图2  亚福莱特拟地花菌菌塘(a)以及周围非菌塘(b)土壤的真菌(A)和细菌(B)的PCoA分析

Fig. 2  Principal coordinate analysis of fungi (A) and bacteria (B) in shiroes (a) soil of Albatrellus flettioides and non-shiroes (b).

2.2 群落组成分析

对各个分类水平上土壤真菌的物种组成进行统计分析。亚福莱特拟地花菌菌塘土壤和非菌塘土壤样品真菌的各个分类水平上的相对丰度有差异(表1，图3)。为了筛选土壤中高丰度真菌类群，相对丰度大于2%的类群被筛选出来，用于后续分析。土壤中的高丰度真菌门为子囊菌门Ascomycota、担子菌门Basidiomycota、毛霉门Mucoromycota、被孢霉门Mortierellomycota、罗兹菌门Rozellomycota、壶菌门Chytridiomycota、球囊菌门Glomeromycota和油壶菌门Olpidiomycota (表1)。土壤的优势真菌纲依次为伞菌纲Agaricomycetes、双担菌纲Geminibasidiomycetes和散囊菌纲Eurotiomycetes。进一步分析土壤中的高丰度真菌目水平的类群(图3)，亚福莱特拟地花菌菌塘和非菌塘土壤样品高丰度真菌目为红菇目Russulales、革菌目Thelephorales、双担菌目Geminibasidiales、伞菌目Agaricales、散囊菌目Eurotiales、阿太菌目Atheliales和牛肝菌目Boletales。真菌高丰度科水平的类群为革菌科Thelephoracea、双担菌科Geminibasidiaceae、地花菌科Albatrellaceae、曲霉科Aspergillaceae、红菇科Russulaceae、角孢革菌科Tylosporaceae和鹅膏菌科Amanitaceae。

表1  基于门水平的亚福莱特拟地花菌菌塘(a)以及周围非菌塘(b)土壤的真菌和细菌的类群统计

Table 1  Statistics of fungi and bacteria in shiroes (a) soil of Albatrellus flettioides and non-shiroes (b) at phylum level

Name of phylumEG (%)CG (%)FungiAscomycota11.3219.5Basidiomycota37.3574.33Mucoromycota1.060.62Mortierellomycota0.271.14Rozellomycota1.32—Chytridiomycota0.010.01Glomeromycota0.000 630.043Olpidiomycota0.006 90.03BacteriaProteobacteria41.1728.89Actinobacteria29.0032.29Acidobacteria11.719.15Firmicutes7.6713.79Gemmatimonadetes3.857.54Chloroflexi1.242.79Planctomycetes1.621.88Verrucomicrobia1.492.43Bacteroidetes1.390.44Elusimicrobia0.030.02Deferribacteres0.040.01Nitrospirae0.001 30.04Deinococcus-Thermus—0.01Aminicenantes0.0050.01Campilobacterota—0.004Thermotogae0.001 30.01Synergistetes0.003 80.003Thermodesulfobacteria0.013 80.004

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图3

图3  亚福莱特拟地花菌菌塘(a)以及周围非菌塘(b)土壤的真菌(A、C、E)和细菌(B、D、F)的多样性组成

Fig. 3  Percentage stack diagram of fungal (A, C, E) and bacterial (B, D, F) families, orders and classes in shiroes (a) soil of Albatrellus flettioides and non-shiroes (b).

对各个分类水平上土壤细菌的物种组成进行统计分析(表1)。土壤中的高丰度细菌门水平的类群包括变形菌门Proteobacteria、放线菌门Actinobacteria、酸杆菌门Acidobacteria、厚壁菌门Firmicutes、芽单胞菌门Gemmatimonadetes、绿弯菌门Chloroflexi、浮霉菌门Planctomycetes、疣微菌门Verrucomicrobia、拟杆菌门Bacteroidetes、迷踪菌门Elusimicrobia、脱铁杆菌门Deferribacteres、硝化螺旋菌门Nitrospirae、异常球菌-栖热菌门Deinococcus-Thermus、Aminicenantes、热袍菌门Thermotogae、互养菌门Synergistetes和热脱硫杆菌门Thermodesulfobacteria。

为了筛选土壤中高丰度细菌纲、目和科水平类群，相对丰度2%的类群被筛选并用于后续分析。菌塘组和非菌塘组中优势菌纲为α变形菌纲Alphaproteobacteria和放线菌纲Actinobacteria。土壤中菌塘组和非菌塘组中高丰度目水平的类群为土壤红杆菌目Solirubrobacterales、粘球菌目Myxococcales、根瘤菌目Rhizobiales、红螺菌目Rhodospirillales、芽单胞菌目Gemmatimonadales、芽孢杆菌目Bacillales和分枝杆菌目Mycobacteriales。菌塘组和非菌塘组中高丰度的真菌科水平的类群为Vicinamibacteraceae、芽单胞菌科Gemmatimonadaceae、伯克霍尔德氏菌科Burkholderiaceae、Anaeromyxobacteraceae、慢生根瘤菌科Bradyrhizobiaceae、分枝杆菌科Mycobacteriaceae和高温单孢菌科Thermomonosporaceae (图3)。

2.3 群落共线性分析和LEfSe分析

按照属水平将真菌丰度排序，绘制前10组的共线性关系图(图4A)。分别为：地花菌属Albatrellus、鹅膏菌属Amanita、Amphinema、双子担子菌属Geminibasidium、青霉属Penicillium、红菇属Russula、乳牛肝菌属Suillus、棉革菌属Tomentella以及未注释组和其他组。其中地花菌属Albatrellus和乳牛肝菌属Suillus与菌塘土壤样品相关性较高，而鹅膏菌属Amanita、Amphinema和红菇属Russula与非菌塘土壤样品具有较高的相关性。

图4

图4  亚福莱特拟地花菌菌塘(a)以及周围非菌塘(b)土壤的真菌(A)和细菌(B)群落属水平共线性关系图

Fig. 4  Collinearity diagram of top 10 bacterial (A) and fungal (B) genera in shiroes (a) soil of Albatrellus flettioides and non-shiroes (b).

同样的方法，将细菌按照属的水平排序，绘制前10组共线性关系图(图4B)。分别为：Actinomarinicola、厌氧黏细菌属Anaeromyxobacter、Baekduia、慢生根瘤菌属Bradyrhizobium、Gemmatirosa、分支杆菌属Mycobacterium、鞘脂单胞菌属Sphingomonas、Vicinamibacter以及未注释组和其他组。其中与亚福莱特拟地花菌菌塘土壤样品相关性较高的细菌类群是慢生根瘤菌属Bradyrhizobium和Vicinamibacter。与非菌塘组非菌塘土壤样品相关性较高的是Actinomarinicola、厌氧黏细菌属Anaeromyxobacter和Gemmatirosa。

进一步进行线性判别分析[line discriminant analysis (LDA) effect size, LEfSe] (图5A)，寻找地花菌塘土壤和非菌塘土壤样品的真菌和细菌的差异类群。在LEfSe分析中，选取丰度大于0.005的类群，共获得2个门、3个纲、9个目、12个科和17个属共43个不同分类水平的真菌指示类群。其中指示类群多数为亚福莱特拟地花菌菌塘土壤中获得的真菌，具有较强指示性(LDA>4, P<0.05)的真菌类群为：刺盾炱目Chaetothyriales、红菇目Russulales、蜡壳耳目Sebacinales、地花菌科Albatrellaceae、地花菌属Albatrellus、支孢瓶霉属Cladophialophora、Herpotrichiellaceae、假绵革菌属Pseudotomentella。

图5

图5  亚福莱特拟地花菌菌塘(a)以及周围非菌塘(b)土壤的真菌(A)和细菌(B)群落LEfSe分析

Fig. 5  LEfSe analyses of fungi (A) and bacteria (B) in shiroes (a) soil of Albatrellus flettioides and non-shiroes (b).

在细菌的LEfSe分析中(图5B)，选取丰度大于0.2的类群，共获得3个门、4个纲、5个目、7个科和9个属共28个不同分类水平的细菌指示类群。其中具有强指示性(LDA>4, P<0.01)的类群为芽单胞菌门Gemmatimonadetes、变形菌门Proteobacteria、α变形菌纲Alphaproteobacteria、芽单胞菌纲Gemmatimonadetes、芽单胞菌目Gemmatimonadales、微球菌目Micrococcales、根瘤菌目Rhizobiales、慢生根瘤菌科Bradyrhizobiaceae、雷兰科Reyranellaceae、芽单胞菌科Gemmatimonadaceae、微球菌科Micrococcaceae、节杆菌属Arthrobacter、慢生根瘤菌属Bradyrhizobium、Gemmatirosa和雷兰属Reyranella。排名前五的指示性真菌类群是变形菌门Proteobacteria、α变形菌纲Alphaproteobacteria、根瘤菌目Rhizobiales、慢生根瘤菌属科Bradyrhizobiaceae和慢生根瘤菌属Bradyrhizobium。

指示性稍弱的细菌类群为厚壁菌门Firmicutes、乙型变形菌纲Betaproteobacteria、δ变形菌纲Deltaproteobacteria、链孢囊菌目Streptosporangiales、黏球菌目Myxococcales、亚硝化单胞菌目Nitrosomonadales、Anaeromyxobacteraceae、高温单孢菌科Thermomonosporaceae、放线菌属Actinomadura、厌氧菌属Anaeromyxobacter和红游动菌属Rhodoplanes。

3 讨论

本研究采用了高通量扩增子测序技术，对云南亚福莱特拟地花菌菌塘及其周边非菌塘土壤真菌和细菌多样性进行了检测，研究发现亚福莱特拟地花菌菌塘土壤的α多样性高于非菌塘土壤，二者在真菌和细菌的结构、群落组成方面存在明显差异。分析了与菌塘组和非菌塘组存在共线性关系的类群，并对指示性类群进行了分析。上述研究为探究适合生长亚福莱特拟地花菌的土壤条件提供了相关证据，明确土壤中部分真菌和细菌对亚福莱特拟地花菌的影响。

本试验中真菌的α多样性明显小于细菌(图1)，这与任丽莹等(2022)的试验结果一致，可能是由于土壤中本身细菌含量多。另外，也可能因为地花菌与云南松根系形成菌根，在有限的资源里限制了其他真菌的生长(王芳和图力古尔 2014)。亚福莱特拟地花菌菌塘土壤的α多样性高于非菌塘土壤，这与Yao et al. (2018)的研究结果一致，菌根真菌与树木形成共生关系，改变了菌塘群落结构，从而加快土壤微生物的碳源代谢，提高了微生物群落的多样性指数。

本次检测到的相对丰度较高的真菌门依次为担子菌门Basidiomycota、子囊菌门Ascomycota、毛霉门Mucoromycota。担子菌门真菌具有降解复杂木质纤维素的能力，因此在许多森林土壤微生物组成的研究中处于优势地位(Lundell et al. 2010；满百膺等 2021)。子囊菌对于环境压力有较好的抵御能力(Egidi et al. 2019)。

本团队通过云南省的野外调查发现，亚福莱特拟地花菌的寄主是云南松。作为建群针叶树种，其外生菌根菌的类群十分丰富，包括红菇属Russula、乳牛肝菌属Suillus、丛枝菌属Ramaria、鹅膏菌属Amanita和棉革菌属Tomentella等多种菌根真菌(于富强等 2003；谢雪丹和刘培贵 2011)，本研究再次验证了这一观点。

在本研究选取的土壤中，真菌丰度排名前几名的属是地花菌属Albatrellus、鹅膏菌属Amanita、Amphinema、双子担子菌属Geminibasidium、青霉属Penicillium、红菇属Russula、乳牛肝菌属Suillus和棉革菌属Tomentella，这几种真菌可能是地花菌潜在的促生菌。其中，棉革菌属Tomentella是很常见的占据主导地位的菌根真菌(谢雪丹和刘培贵 2011)，常与云南松形成菌根(Haug et al. 2005；Jakucs & Erős-Honti 2008)。另外2个属，芽单胞菌属Gemmatimonas和鞘脂单胞菌属Sphingomonas能够促进植物对氮的代谢转化(Chen et al. 2014；Rincón-Molina et al. 2019；Liu et al. 2021)。另外，在目水平上，红菇目真菌是丰度最大的类群，原因可能是云南松幼苗喜好光照水分充足且土壤养分充足的地方，该环境条件有利于形成直接接触型或者短距离探索型的菌根如红菇类真菌，该类真菌较容易与云南松形成菌根(谢雪丹等 2010)。共线性关系分析显示鹅膏菌属与非菌塘土壤相关性更大，原因可能是鹅膏菌属与拟地花菌属占据相同的生态位，地花菌率先与云南松形成菌根，占据了鹅膏菌真菌的养分来源从而抑制了鹅膏菌菌丝的产生。

在细菌丰度分析中，Actinomarinicola、厌氧黏细菌属Anaeromyxobacter、Baekduia、慢生根瘤菌属Bradyrhizobium、Gemmatirosa、分支杆菌属Mycobacterium、鞘脂单胞菌属Sphingomonas和Vicinamibacter占比较多，这与伍燕等(2021)的研究结果类似。慢生根瘤菌属Bradyrhizobium是典型的固氮细菌(Ormeño-Orrillo et al. 2012)，而雷兰属Reyranella是反硝化细菌(Lee et al. 2017)，二者均存在于亚福莱特拟地花菌菌塘土壤样品中，与其参与土壤氮循环有关。

综合以上分析，尤其是共线性分析与指示性物种的分析以及之前的研究结果，推测慢生根瘤菌属Bradyrhizobium、乳牛肝菌属Suillus和芽单胞菌属Gemmatimonas可能是亚福莱特拟地花菌潜在属水平的促生菌，可为探究拟地花菌的生长环境以及地花菌属珍稀物种的种质资源保护提供理论基础。

致谢

感谢戴玉成老师在样品采集工作中的支持，感谢李婉莹和刘鸿参与研究样品的采集工作。

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Phaeolus schweinitzii (Fr.) Pat. was originally described in Europe and is considered a common forest pathogen on conifers in the Northern Hemisphere. Our molecular phylogeny based on samples from China, Europe, and North America confirms that P. schweinitzii is a species complex, including six taxa. P. schweinitzii sensu stricto has a distribution in Eurasia; the samples from Northeast and Southwest China are distantly related to P. schweinitzii sensu stricto, and two new species are described after morphological, phylogenetic, and geographical analyses. The species growing on Larix, Picea, and Pinus in Northeast China is described as Phaeolus asiae-orientalis. Another species mostly occurring on Pinus yunnanensis in Southwest China is Phaeolus yunnanensis. In addition, three taxa distributed in North America differ from P. schweinitzii sensu stricto. Phaeolus tabulaeformis (Berk.) Pat. is in Southeast North America, “P. schweinitzii-1” in Northeast North America, and “P. schweinitzii-2” in western North America.

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