Biodiversity Science ›› 2019, Vol. 27 ›› Issue (8): 842-853.doi: 10.17520/biods.2019034

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Genetic diversity and toxin-producing characters of Aspergillus flavus from China

Zhongdong Yu1, Zhihe Yu2, Shiyu Jin3, Long Wang4, *()   

  1. 1. College of Forestry, Northwest A & F University, Yangling, Shaanxi 712100;
    2. College of Life Sciences, Yangtze University, Jingzhou, Hubei 434025
    3. Beijing Jingxi Forest Farm, Mentougou, Beijing 102300
    4. State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101
  • Received:2019-02-14 Accepted:2019-05-15 Online:2019-05-20
  • Wang Long

Aspergillus flavus is commonly regarded as a kind of saprophytic fungi with a wide distribution. It is the major aflatoxin B (AFB) and cyclopiazonic acid (CPA) producing species, as well as a pathogen to humans and animals. In the world, huge amounts of corns, peanuts and cotton seeds are vulnerable to be contaminated by A. flavus and aflatoxin each year. There is much variance in morphological, genetic and toxin-producing characters among isolates of A. flavus, resulting in its ambiguous population structure. In this paper, we analyzed 88 isolates of A. flavus from different environments of 26 provinces (including the Greater and Lesser Khinggan Mountains) in China, as well as nine ex-types and authentic strains based on CaM and benA sequences to infer their sequence types (STs) using multi-locus sequence typing (MLST), and their phylogenetic relationships and population structures employing MEGA 6.0 and Structure 2.3.4 softwares, together with their toxin-producing features (AFB and CPA). Our results showed that the 88 Chinese isolates and nine ex-type and authentic strains were distributed in three populations, i.e. A. flavus population I, A. flavus population II and population A. oryzae. There were 17 STs among the 97 isolates, among which the 88 strains from China were distributed in 15 STs. All isolates of population A. oryzae did not produce AFB, but most isolates of the A. flavus populations I and II produced AFB and CPA. The toxin-producing features were strain-specific, but not correlated to sequence types or populations. Some correlations between toxin-producing characters and geographical environments or crop types were recognized. The isolates of A. flavus populations I and II from the northeast areas planting corns, the arid northwest planting cottons and the south areas growing peanuts all produced AFB and CPA. The isolates from Hoh Xil of Qinghai and Aba of Sichuan did not produce AFB, though with the production of CPA. The isolates of A. oryzae population without AFB production were almost from North China with diverse climates and geographical environments, where the traditional Chinese soybean paste is made in the rural areas.

Key words: diversity, genetic markers, mycotoxins, orthologous genes, phylogenetics

Table 1

Aspergillus flavus strains, isolation places and toxin-production"

Isolation places and substrates
Toxin production
1 A. flavus CBS 100927T 南太平洋群岛; 赛璐玢 Cellophane; South Pacific Islands - +
2 A. oryzae CBS 100925T 日本大阪; 分离基物未知
Ex-type of A. oryzae, unknown source; Osaka, Japan
- +
3 A. thomii CBS 120.51T 英国伦敦; 污染物 Ex-type of A. thomii, culture contaminant; London, UK - +
4 A. flavus CYH2-2-1 河北石家庄; 空气 Air; Shijiazhuang, Hebei, China + +
5 A. flavus 3.4408 日本东京; 土壤 Soil; Tokyo, Japan + +
6 A. flavus 14527 西藏米林; 土壤 Soil; Milin, Tibet, China + +
7 A. flavus 13483 山西五台山; 土壤 Soil; Mt. Wutaishan, Shanxi, China + +
8 A. flavus 13868 内蒙古呼伦贝尔; 土壤 Soil; Hulun Buir, Inner Mongolia, China + +
9 A. flavus 13894 湖南益阳; 土壤 Soil; Yiyang, Hunan, China + +
10 A. flavus 13895 江西三清山; 土壤 Soil; Sanqingshan, Jiangxi, China + +
11 A. flavus 13918 江苏苏州; 土壤 Soil, Suzhou, Jiangsu, China + +
12 A. flavus 13952 甘肃兰州; 土壤 Soil; Lanzhou, Gansu, China - +
13 A. flavus 13961 宁夏罗山; 土壤 Soil; Luoshan, Ningxia, China - -
14 A. flavus 13962 宁夏灵武; 土壤 Soil; Lingwu, Ningxia, China - -
15 A. flavus 14099 山西吕梁; 土壤 Soil; lvliang, Shanxi, China + +
16 A. flavus 14131 山西大同; 土壤 Soil; Datong, Shanxi, China + +
17 A. flavus 14151 河南洛阳; 土壤 Soil; Luoyang, Henan, China - -
18 A. flavus 14152 河南南阳; 土壤 Soil; Nanyang, Henan, China - -
19 A. flavus 14153 山东泰安 土壤 Soil; Tai’an, Shandong, China - -
20 A. flavus 14154 山东临沂; 土壤 Soil; Linyi, Shandong, China - -
21 A. flavus 14155 河北兴隆; 土壤 Soil; Xinglong, Hebei, China - -
22 A. flavus 14156 河北张家口; 土壤 Soil; Zhangjiakou, Hebei, China - -
23 A. flavus 14157 河北保定; 土壤 Soil; Baoding, Hebei, China - -
24 A. flavus 14159 河北衡水; 土壤 Soil; Hengshui, Hebei, China - -
25 A. flavus 14175 浙江乌镇; 土壤 Soil; Wuzhen, Zhejiang, China + +
26 A. flavus 14334 安徽巢湖; 荸荠 Water chestnut; Chaohu, Anhui, China + +
27 A. flavus 14353 新疆吐鲁番; 土壤 Soil; Turpan, Xinjiang, China + +
28 A. flavus 14355 新疆石河子; 土壤 Soil; Shihezi, Xinjiang, China + +
29 A. flavus 14356 新疆乌鲁木齐; 土壤 Soil; Urumqi, Xinjiang, China + +
30 A. flavus 14357 新疆伊犁; 土壤 Soil; Yili, Xinjiang, China + +
31 A. flavus 14358 陕西榆林; 土壤 Soil; Yulin, Shaanxi, China + +
32 A. flavus 14359 陕西汉中; 土壤 Soil; Hanzhong, Shaanxi, China + +
33 A. flavus 14373 陕西渭南; 土壤 Soil; Weinan, Shaanxi, China + +
34 A. flavus 14374 新疆吐鲁番; 土壤 Soil, Turpan, Xinjiang, China + +
35 A. flavus 23124 海南五指山; 土壤 Soil; Mt. Wuzhishan, Hainan, China + +

Table 1


Isolation places and substrates
Toxin production
36 A. flavus AB34 四川若尔盖; 土壤 Soil; Ruoergai Prairie, Sichuan, China - +
37 A. flavus FJ17-2 福建宁德; 茶叶 Tea; Ningde, Fujian, China + +
38 A. flavus HB4 湖北神农架; 土壤 Soil; Shennongjia, Hubei, China + +
39 A. flavus HL53 黑龙江凉水; 土壤 Soil; Liangshui Nature Reserve, Heilongjiang, China + +
40 A. flavus HL70 黑龙江乌伊岭; 土壤 Soil; Wuyiling, Heilongjiang, China + +
41 A. flavus KK39 青海互助县; 土壤 Soil; Huzhu County, Qinghai, China - +
42 A. flavus KK41 青海互助县; 土壤 Soil; Huzhu County, Qinghai, China - +
43 A. flavus KK49 青海互助县; 土壤 Soil; Huzhu County, Qinghai, China - +
44 A. flavus KK50 青海可可西里; 土壤 Soil; Hoh Xil, Qinghai, China - +
45 A. flavus KK65 青海楚玛尔河; 土壤 Soil; Chumaer River, Qinghai, China - +
46 A. flavus KK66 青海可可西里; 土壤 Soil; Hoh Xil, Qinghai, China - +
47 A. flavus KK67 青海楚玛尔河; 土壤 Soil; Chumaer River, Qinghai, China - +
48 A. flavus KK68 青海沱沱河; 土壤 Soil; Tuotuo River, Qinghai, China - +
49 A. flavus KK69 青海沱沱河; 土壤 Soil; Tuotuo River, Qinghai, China - +
50 A. flavus KK70 青海楚玛尔河; 土壤 Soil; Chumaer River, Qinghai, China - +
51 A. flavus KK72 青海青海湖; 土壤 Soil; Qinghai Lake, Qinghai, China + +
52 A. flavus KK73 青海青海湖; 土壤 Soil; Qinghai Lake, Qinghai, China + +
53 A. flavus KK94 青海坎布拉; 土壤 Soil; Kanbula, Qinghai, China + +
54 A. flavus KK102 青海坎布拉; 土壤 Soil; Kanbula, Qinghai, China - +
55 A. flavus KK103 青海坎布拉; 土壤 Soil; Kanbula, Qinghai, China - +
56 A. flavus KK104 青海坎布拉; 土壤 Soil; Kanbula, Qinghai, China - +
57 A. flavus KK114 青海坎布拉; 土壤 Soil; Kanbula, Qinghai, China - +
58 A. flavus XZ107 陕西南宫山; 植物叶 Plant leaves; Mt. Nangongshan, Shaanxi, China + +
59 A. flavus XZ108 陕西通天河; 植物叶 Plant leaves; Tongtian River, Shaanxi, China + +
60 A. flavus XZ109 陕西南宫山; 植物叶 Plant leaves; Mt. Nangongshan, Shaanxi, China + +
61 A. flavus XZ112 陕西通天河; 植物叶 Plant leaves; Tongtian River, Shaanxi, China + +
62 A. flavus YN23 云南玉溪; 烟叶 Tobacco leaves; Yuxi, Yunnan, China - +
63 A. flavus YN35 云南玉溪; 烟叶 Tobacco leaves; Yuxi, Yunnan, China + +
64 A. flavus YN48 云南玉溪; 烟叶 Tobacco leaves; Yuxi, Yunnan, China + +
65 A. flavus YN49 云南玉溪; 烟叶 Tobacco leaves; Yuxi, Yunnan, China + +
66 A. flavus YN51 云南玉溪; 烟叶 Tobacco leaves; Yuxi, Yunnan, China + +
67 A. flavus NRRL 3357 美国; 霉花生 Moldy peanuts; USA + +
68 A. oryzae RIB40 日本; 谷粒 Cereal grains; Japan - -
69 A. flavus 3.262 辽宁大连; 空气 Air; Dalian, Liaoning, China - -
70 A. flavus 3.267 辽宁大连; 土壤 Soil; Dalian, Liaoning, China - +
71 A. flavus 3.337 天津; 蚊香 Mosquito-repellent incense; Tianjin, China - +
72 A. flavus 3.417 天津; 酱曲 Soy sauce starter; Tianjin, China - +
73 A. flavus 3.870 天津; 酱曲 Soy sauce starter; Tianjin, China + +
74 A. flavus 3.881 上海; 小麦 Wheat; Shanghai, China - +
75 A. flavus 3.2146 北京; 大米 Rice; Beijing, China + +
76 A. flavus 3.2758 广东广州; 空气 Air; Guangzhou, Guangdong, China - +
77 A. flavus 3.2789 越南河内; 土壤 Soil; Hanoi, Vietnam - +
78 A. flavus 3.2823 安徽芜湖; 植物 Plants; Wuhu, Anhui, China - +

Table 1


Isolation places and substrates
Toxin production
79 A. flavus 3.3554 北京; 空气 Air; Beijing, China - +
80 A. flavus var. columnaris CBS 485.65T 日本; 黄油 Ex-type of A. flavus var. columnaris, butter; Japan - +
81 A. flavus 3.4408-2 北京; 空气 Air; Beijing, China + +
82 A. flavus 3.4410 美国 ATCC 28539; USA + +
83 A. flavus 3.5211 北京 CICC 2348; Beijing, China - +
84 A. flavus 3.5278 四川德阳; 烂水果 Rotten fruit; Deyang, Sichuan, China + +
85 A. flavus 3.5283 四川成都; 土壤 Soil; Chengdu, Sichuan, China + +
86 A. flavus 3.5309 四川都江堰; 土壤 Soil; Dujiangyan, Sichuan, China + +
87 A. flavus 3.5329 贵州梵净山; 皮革 Leather; Mt. Fanjingshan, Guizhou, China + +
88 A. flavus 3.6153 山东泰安; 小麦 Wheat; Tai’an, Shandong, China - +
89 A. flavus 3.6304 广西宜山; 玉米 Corn; Yishan, Guangxi, China - +
90 A. flavus 3.6307 吉林珲春; 亚麻 Linen; Hunchun, Jilin, China + +
91 A. flavus 3.6311 广东广州; 空气 Air; Guangzhou, Guangdong, China + +
92 A. flavus 3.6422 河北小五台山; 松果 Pinecore; Mt. Small Wutaishan, Hebei, China + +
93 A. flavus 3.6428 云南大理; 霉纸 Mouldy paper; Dali, Yunnan, China + +
94 A. flavus 3.6431 云南大理; 玉米叶 Corn leaves; Dali, Yunnan, China + +
95 A. flavus 3.6434 云南思茅; 土壤 Soil; Simao, Yunnan, China - +
96 A. flavus 14160 河南信阳; 土壤 Soil,; Xinyang, Henan, China - -
97 A. flavus FJ17 福建宁德; 茶叶 Tea; Ningde, Fujian, China + +
A. arachidicola CBS 117610T 阿根廷; 花生叶 Arachis glabrata leaves; Argentina
A. minisclerotigenes CBS 115635T 阿根廷; 花生 Arachis hypogaea seeds; Argentina
A. parasiticus CBS 100926T 美国夏威夷; 嗜桔粉蚧 Pseudococcus calceolariae; Hawaii, USA
3.306 天津; 酱曲 Soy sauce starter; Tianjin, China
A. aflatoxiformans CBS 143679T 尼日利亚; 土壤 Soil; Nigeria
A. tamarii CBS 104.13T 分离地未知; 活性碳 Activated carbon; unknown country

Fig. 1

The maximum likelihood phylogram of 97 Aspergillus flavus strains and its four close-related species. The ex-type of A. flavus CBS 100927T, ex-type of A. flavus var. columnaris CBS485.65T, ex-type of A. oryzae CBS 100925T, and ex-type of A. thomii CBS 120.51T are in the same clade with a 92% support, with the ex-type of A. tamari CBS 104.13T as the outgroup. The red, green and blue colours are in accordance with Fig. 3."

Table 2

The best population number K inferred by Structure 2.3.4"

K Replicates Mean LnP(K) Stdev LnP(K) Ln°(K) |Ln?(K)| Delta K
2 20 -252.900000 11.116323 - - -
3 20 -153.585000 0.665918 99.315000 115.770000 173.850119
4 20 -170.040000 4.371607 -16.455000 14.975000 3.425514
5 20 -171.520000 3.293790 -1.480000 16.860000 5.118723
6 20 -189.860000 14.895474 -18.340000 402.695000 27.034721
7 20 -610.895000 1,768.728466 -421.035000 779.785000 0.440873
8 20 -252.145000 53.166892 358.750000

Fig. 2

The best population numbers calculated by Structure Harvester (the best number is 3 for delta K)"

Fig. 3

The three populations of the 97 Aspergillus flavus isolates calculated by Structure Harvester. Red, green and blue colours stand for the three different populations, each column stands for each strain, and the number under each column is in accordance with those in Table 1."

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