Biodiversity Science ›› 2018, Vol. 26 ›› Issue (12): 1308-1317.doi: 10.17520/biods.2018131

• Original Papers • Previous Article     Next Article

Species diversity and vertical distribution characteristics of Metarhizium in Gaoligong Mountains, southwestern China

Zihong Chen1, Xiaona Yang1, Ningjing Sun1, Ling Xu1, *(), Yuan Zheng2, Yuming Yang3   

  1. 1 Institute of Biological Resources of Gaoligong Mountains, Baoshan University, Baoshan, Yunnan 678000
    2 College of Forestry, Southwest Forestry University, Kunming 650224
    3 Key Laboratory of Forest Plant Cultivation and Utilization, Yunnan Academy of Forestry, Kunming 650201
  • Received:2018-05-03 Accepted:2018-07-04 Online:2019-02-11
  • Xu Ling
  • About author:# 同等贡献作者 Contributed equally to this work

Gaoligong Mountains in Yunnan Province, China have diverse ecological systems and biological resources. To understand the diversity and the vertical distribution of Metarhizium species at different elevations in this area, Metarhizium resources were investigated in seven typical vegetation types (i.e., I, dry-hot valley; II, monsoon evergreen broad-leaved forest; III, warm coniferous forest; IV, mod-montane humid evergreen broad-leaved forest; V, mountain moss dwarf forest; VI, cold shrubs of meadow; and VII, rocky beach sparsely vegetation) along an elevation gradient (600-3,800 m). Strains of Metarhizium were isolated from soils of the vegetations at different elevations and identified using multi-gene (nrSSU, nrLSU, EF-1α, RPB1, and RPB2) phylogenetic analysis. Our result indicated that the species of Metarhizium in Gaoligong Mountains were abundant and the obtained 161 strains represented 12 Metarhizium species, namely, M. rileyi, M. viridulum, M. lepidiotae, M. brunneum, M. pingshaense, M. anisopliae, M. robertsii, M. guizhouense, M. indigoticum, M. pemphigi, M. campsosterni, and Metacordyceps neogunnii, and most of them (8 species) belonged to M. anisopliae complex. Additionally, Nigelia martiale, a taxon close to Metarhizium was also found in this area. M. indigoticum is new to China. Fungi of Metarhizium in Gaoligong Mountains were widely distributed in six vegetation types at elevation between 600 m and 3,400 m, but not in type VII at the elevation of 3,600-3,800 m. The vegetations at the low and middle elevations (I-IV) harbored larger number of strains (≥ 23) and higher species diversity (4-9 species), whereas those at high elevations (V-VI) possessed fewer strains (2-8) and relatively limited species (1-2 species). Metarhizium resources were the most abundant in evergreen broad-leaved forests at the middle elevation. The monsoon evergreen broad-leaved forest (vegetation type II) possessed the largest number of Metarhizium strains (52 strains, 32.3% of the total) and species (9 species), while mid-montane humid evergreen broad-leaved forest (vegetation type IV) (47 strains, 29.2% of the total) was the next. The superior species phenomenon of Metarhizium was remarkable in Gaoligong Mountains, M. brunneum being the most dominant, at 46.6% of the total strain numbers. It widely exists in six vegetation types (I-VI) with very different habitat conditions, suggesting that this species has the highest ecologic adaptability.

Key words: Gaoligong Mountains, Metarhizium, phylogenetic analysis, species diversity, vertical distribution

Fig. 1

Colonies of Metarhizium species and other fungal materials in Gaoligong Mountains. (A) Colony of M. brunneum; (B) Colony of M. lepidiotae; (C) Colony of M. indigoticum; (D) Colony of M. campsosterni; (E) Colony of M. robertsii; (F) Colony of M. guizhouense; (G) Colony of M. anisopliae; (H) Colony of M. pingshaense; (I) Colony of M. viridulum; (J) Colony of M. pemphigi; (K) Colony of M. rileyi; (L) Colony of Mc. neogunnii; (M) The induction and isolation of Metarhizium; (N) Stroma of M. viridulum; (O) Spores of M. rileyi on the infected Lepidoptera larva; (P) Spores of M. pemphigi on the infected beetle larva; (Q) Fruit body of N. martiale. Bar of A-O and Q = 1 cm; Bar of P = 0.5 cm."

Table 1

Strain numbers and habitat conditions of Metarhizium species in Gaoligong Mountains. I, Dry-hot valley; II, Monsoon evergreen broad-leaved forest; III, Warm coniferous forest; IV, Mid-montane humid evergreen broad-leaved forest; V, Mountain moss dwarf forest; VI, Cold shrubs of meadow; VII, Rocky beach sparsely vegetation."

strain number
Vegetation type
Altitude span (m)
Temperature (℃)
Humidity (%)
Metarhizium brunneum 75 46.6 I-VI 600-3,400 13-34 32-80
M. pemphigi 25 15.5 I, II, IV 800-2,119 20-32 39-70
M. pingshaense 11 6.8 I, IV, V 1,925-3,135 15-34 58-74
M. guizhouense 13 8.1 II, IV 1,540-2,280 18-30 57-74
M. rileyi 10 6.2 II, IV 1,780-2,495 17-27 49-54
M. robertsii 5 3.1 I, IV 723-1,981 22-32 52-63
M. indigoticum 4 2.5 II, III 1,512-1,981 22-30 58-59
M. anisopliae 4 2.5 II, III 1,370-1,900 25-30 60-76
Metacordyceps neogunnii 7 4.4 II 1,438 25 65
M. campsosterni 5 3.1 IV 2,022 22 58
M. viridulum 1 0.6 II 1,540 30 57
M. lepidiotae 1 0.6 III 1,765 25 58
Nigelia martiale - - II 1,568 30 60
合计 Total 161 100 6 600-3,400 13-34 32-80

Fig. 2

Phylogenetic tree of Metarhizium based on nucleotide sequences of five loci (nrSSU, nrLSU, EF-1α, RPB1and RPB2) dataset. Those from Gaoligong Mountains are marked in bold."

Fig. 3

Morphology of the new record species in China, Metarhizium indigoticum (strain BUM 1512.8). (A) Obverse of the colony on PPDA; (B) Reverse of the colony on PPDA; (C) Conidia chains; (D, E) Conidiogenous structures. Bar of C-E = 5 µm."

Fig. 4

Species and strain numbers of Metarhizium in different vegetation types of Gaoligong Mountains. L, Low elevation; M, Middle elevation; H, High elevation."

1 Bischoff JF, Rehner SA, Humber RA (2006) Metarhizium frigidum sp. nov.: A cryptic species of M. anisopliae and a member of the M. flavoviride complex. Mycologia, 98, 737-745.
2 Bischoff JF, Rehner SA, Humber RA (2009) A multilocus phylogeny of the Metarhizium anisopliae lineage. Mycologia, 101, 512-530.
3 Chen MJ (2008) Study on Biodiversity of Entomogenous Fungi in Different Forest Ecosystems. PhD dissertation, Anhui Agricultural University, Hefei>. (in Chinese with English abstract)
[陈名君 (2008) 不同森林生态系虫生真菌生物多样性研究. 博士学位论文, 安徽农业大学, 合肥.]
4 Chen ZH, Dai YD, Yu H, Yang K, Yang ZL, Yuan F, Zeng WB (2013) Systematic analyses of Ophiocordyceps lanpingensis sp. nov., a new species of Ophiocordyceps in China. Microbiological Research, 168, 525-532.
5 Chu HL, Chen WH, Wen TC, Liang ZQ, Zheng FC, Liang JD, Han YF (2016) Delimitation of a novel member of genus Metarhizium (Clavicipitaceae) by phylogenetic and network analysis. Phytotaxa, 288, 51-60.
6 Driver F, Milner RJ, Trueman WH (2000) A taxonomic revision of Metarhizium based on a phylogenetic analysis of rDNA sequence data. Mycological Research, 104, 134-150.
7 Guo HL, Ye BL, Qiu YY, Chen QT, Fu CS (1986) Three new species of Metarhizium. Mycosystema, 5, 177-184. (in Chinese)
[郭好礼, 叶柏龄, 邱莹玉, 陈庆涛, 付仓生 (1986) 绿僵菌属的三个新种. 菌物学报, 5, 177-184.]
8 He R, Yang W, Li YY, Chai Y, Fang B (2004) Study on soil character of two forest types in southern part of Gaoligong Mountains. Journal of West China Forestry Science, 33(3), 46-52. (in Chinese)
[何蓉, 杨卫, 李玉媛, 柴勇, 方波 (2004) 高黎贡山南段2种森林类型的土壤特性研究. 西部林业科学, 33(3), 46-52.]
9 Huang B, Li SG, Li CR, Fan MZ, Li ZZ (2004) Studies on the taxonomic status of Metarhizium cylindrospora and Nomuraea viridula. Mycosystema, 23, 33-37. (in Chinese with English abstract)
[黄勃, 李世贵, 李春如, 樊美珍, 李增智 (2004) 柱孢绿僵菌和绿色野村菌分类地位的研究. 菌物学报, 23, 33-37.]
10 Huang GQ, Zhang ZS, Liu YH (2017) Review of the comb-tailed spider genus Hahnia C. L. Koch 1841 (Hahniidae) from Gaoligong Mountains in Yunnan, China. Zootaxa, 4344, 444-464.
11 Kavanaugh DH, Hieke F, Liang HB, Dong DZ (2014) Inventory of the carabid beetle fauna of the Gaoligong Mountains, western Yunnan Province, China: Species of the tribe Zabrini (Coleoptera, Carabidae). Zookeys, 407, 55-119.
12 Kepler RM, Humber RA, Bischoff JF, Rehner SA (2014) Clarification of generic and species boundaries for Metarhizium and related fungi through multigene phylogenetics. Mycologia, 106, 811-829.
13 Kepler RM, Sung GH, Ban S, Nakagiri A, Chen MJ, Huang B, Li Z, Spatafora JW (2012) New teleomorph combinations in the entomopathogenic genus Metacordyceps. Mycologia, 104, 182-197.
14 Keyser CA, Licht HHDF, Steinwender BM, Meyling NV (2015) Diversity within the entomopathogenic fungal species Metarhizium flavoviride associated with agricultural crops in Denmark. BMC Microbiology, 15, 249.
15 Li CR, Huang B, Fan MZ, Lin YG, Li ZZ (2010) Metacordyceps guniujiangensis and its Metarhizium anamorph: A new pathogen on cicada nymphs. Mycotaxon, 111, 221-231.
16 Li R, Dao ZL, Li H (2011) Seed plant species diversity and conservation in the northern Gaoligong Mountains in western Yunnan, China. Mountain Research and Development, 31, 160-165.
17 Liang ZQ (2007) Flora Fungorum Sinicorum, Vol. 32: Cordyceps. Science Press, Beijing. (in Chinese)
[梁宗琦 (2007) 中国真菌志(第32卷): 虫草属. 科学出版社, 北京.]
18 Liang ZQ, Liu AY, Liu JL (1991) A new species of the genus Cordyceps and its Metarhizium anamorph.Mycosystema, 10, 257-262. (in Chinese)
[梁宗琦, 刘爱英, 刘杰麟 (1991) 虫草一新种及其绿僵菌无性型. 菌物学报, 10, 257-262.]
19 Liu ZY, Liang ZQ, Whalley AJS, Yao YJ, Liu AY (2001) Cordyceps brittlebankisoides, a new pathogen of grubs and its anamorph, Metarhizium anisopliae var. majus. Journal of Invertebrate Pathology, 78, 178-182.
20 Luangsa-ard JJ, Mongkolsamrit S, Thanakitpipattana D, Khonsanit A, Tasanathai K, Noisripoom W, Humber RA (2017) Clavicipitaceous entomopathogens: New species in Metarhizium and a new genus Nigelia. Mycological Progress, 16, 369-391.
21 Nishi O, Shimizu S, Sato H (2017) Metarhizium bibionidarum and M. purpureogenum: New species from Japan. Mycological Progress, 16, 987-998.
22 Sharma SK, Gautam N (2015) Metacordyceps dhauladharensis sp. nov., a new entomopathogenic fungus from India. Turkish Journal of Botany, 39, 520-526.
23 Spatafora JW, Sung G-H, Sung JM, Hywel-Jones NL, White JF Jr (2007) Phylogenetic evidence for an animal pathogen origin of ergot and the grass endophytes. Molecular Ecology, 16, 1701-1711.
24 Su WP, Du F, Yang YM, Wang J (2014) The flora on mid-mountain humid evergreen broadleaf forest of the southern part of Mt. Gaoligongshan. Journal of Yunnan Agricultural University, 29, 792-798. (in Chinese with English abstract)
[苏文苹, 杜凡, 杨宇明, 王娟 (2014) 高黎贡山南段中山湿性常绿阔叶林植物区系研究. 云南农业大学学报, 29, 792-798.]
25 Sung GH, Hywel-Jones NL, Sung JM, Luangsa-ard JJ, Shrestha B, Spatafora JW (2007) Phylogenetic classification of Cordyceps and the clavicipitaceous fungi. Studies in Mycology, 57(1), 5-59.
26 Tulloch M (1976) The genus Metarhizium. Transactions of the British Mycological Society, 66, 407-411.
27 Wang M, Yin YP, Wang ZK (2014) Multilocus phylogenetic analysis of the taxonomic status of 10 strains of Metarhizium. Plant Protection, 40(5), 14-21. (in Chinese with English abstract)
[王萌, 殷幼平, 王中康 (2014) 10株绿僵菌菌株分类地位的多基因系统进化分析. 植物保护, 40(5), 14-21.]
28 Wen TC, Xiao YP, Han YF, Huang SK, Zha LS, Hyde KD, Kang JC (2017) Multigene phylogeny and morphology reveal that the Chinese medicinal mushroom ‘Cordyceps gunnii’ is Metacordyceps neogunnii sp. nov. Phytotaxa, 302, 27-39.
29 Wen TC, Zha LS, Xiao YP, Wang Q, Kang JC, Hyde KD (2015) Metacordyceps shibinensis sp. nov. from larvae of Lepidoptera in Guizhou Province, southwest China. Phytotaxa, 226, 51-62.
30 Xu CD, Feng JM, Wang XP, Yang X (2008) Vertical distribution patterns of plant species diversity in northern Mt. Gaoligong, Yunnan Province. Chinese Journal of Ecology, 27, 323-327. (in Chinese)
[徐成东, 冯建孟, 王襄平, 杨雪 (2008) 云南高黎贡山北段植物物种多样性的垂直分布格局. 生态学杂志, 27, 323-327.]
31 Zhang WM, Hu B, Zhong H, Chen YQ, Tao MH, Qu LH (2005) Study on the anamorph of Cordyceps campsosterna. In: Proceedings of the First Symposium on Development of China’s Medicinal Fungi Industry (ed. Mycological Society of China), pp. 81-82. Nantong, Jiangsu. (in Chinese)
[章卫民, 胡泊, 钟韩, 陈月琴, 陶美华, 屈良鹄 (2005) 丽叩甲虫草(Cordyceps campsosterna)无性型的研究. 见: 首届药用真菌产业发展暨学术研讨会论文集(中国菌物学会), pp. 81-82. 江苏南通.]
32 Zhou H (2008) Studies on the Diversity of Soil Microorganisms in Gaoligongshan National Nature Reserve, Yunnan. PhD dissertation, Hunan Agricultural University, Changsha. (in Chinese with English abstract)
[周慧 (2008) 云南高黎贡山国家自然保护区土壤微生物多样性研究. 博士学位论文, 湖南农业大学, 长沙.]
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