不同盐度培养下海洋真菌Aspergillus unguis DLEP2008001生物活性及次生代谢组变化

doi:10.13560/j.cnki.biotech.bull.1985.2024-0150

生物技术通报 ›› 2024, Vol. 40 ›› Issue (11): 296-311.doi: 10.13560/j.cnki.biotech.bull.1985.2024-0150

不同盐度培养下海洋真菌Aspergillus unguis DLEP2008001生物活性及次生代谢组变化

康晓博¹(), 张璟汐¹, 卢甜甜¹, 刘亚月¹^,², 周龙建¹^,², 张翼¹^,²^,³()

1.广东海洋大学食品科技学院广东省水产品加工与安全重点实验室广东省海洋生物制品工程实验室广东海洋大学深圳研究院海洋医药研发中心湛江市脑健康相关海洋药物与营养品重点实验室，湛江 524088
2.南方海洋科学与工程广东省实验室（湛江），湛江 524006
3.海洋食品精深加工关键技术省部共建协同创新中心大连工业大学，大连 116034

收稿日期:2024-02-11 出版日期:2024-11-26 发布日期:2024-12-19
通讯作者: 张翼，男，博士，教授，研究方向：海洋天然产物；E-mail: hubeizhangyi@163.com
作者简介:康晓博，男，硕士研究生，研究方向：海洋生物活性物质；E-mail: k17701892041@126.com
第一联系人：
张璟汐为本文共同第一作者
基金资助:
广东省基础与应用基础研究基金自然科学基金（面上项目）(2022A1515010783);广东省普通高校重点领域专项（生物医药与健康）(2021ZDZX2064);深圳市科创委基础研究面上项目(JCYJ20220530162014032);湛江市海洋青年人才创新项目(2022E05010);广东海洋大学大学生创新创业训练计划项目(S202110566014);广东海洋大学研究生教育创新计划项目(202232)

Variation of Bioactivities and Secondary Metabolomics of Marine Fungus Aspergillus unguis DLEP2008001 Cultured under Different Salinities

KANG Xiao-bo¹(), ZHANG Jing-xi¹, LU Tian-tian¹, LIU Ya-yue¹^,², ZHOU Long-jian¹^,², ZHANG Yi¹^,²^,³()

1. College of Food Science and Technology, Guangdong Ocean University, Guangdong Provincial Key Laboratory of Aquatic Product Processing and Safety, Marine Biomedicine Research & Development Center at Shenzhen Institute of Guangdong Ocean University, Zhanjiang Municipal Key Laboratory of Marine Drugs and Nutrition for Brain Health, Zhanjiang 524088
2. Southern Marine Science and Engineering Guangdong Laboratory（Zhanjiang）, Zhanjiang 524006
3. Collaborative Innovation Center of Seafood Deep Processing, Dalian Polytechnic University, Dalian 116034

Received:2024-02-11 Published:2024-11-26 Online:2024-12-19

摘要/Abstract

摘要：

【目的】 以一株海洋真菌爪曲霉Aspergillus unguis DLEP2008001为对象，研究不同盐度对其生物活性和次生代谢产物的影响。【方法】 对不同盐度培养下该菌株第14天和第28天的固体和液体培养基发酵产物提取物，分别采用薄层层析和抗氧化、乙酰胆碱酯酶抑制及抗菌生物活性自显影手段，分析其活性次生代谢产物差异，将样品进一步采用高效液相色谱以及基于液相色谱串联质谱的“多途径辅助的特征分子网络”代谢组学分析手段，系统地研究不同盐度培养下A. unguis DLEP2008001次生代谢产物的多样性变化。【结果】 盐度可以调节抗氧化、抑制乙酰胆碱酯酶以及抗菌活性成分的产量与多样性，采用海水马铃薯蔗糖液体培养基28 d培养时在35 g/L盐度下出现最为丰富的特征代谢产物，而大米固体培养基在5 g/L盐度下特征代谢产物最为丰富、35 g/L盐度下也较丰富，固体发酵优势代谢产物的平均分子量随着盐度上升而总体呈现下降趋势，该菌株在高盐条件下的优势代谢产物多为含多羟基、多氨基的小分子化合物，推测可能参与渗透压调节。【结论】 提取物盐度对该爪曲霉菌株的生物活性及次生代谢产物有显著的影响。

关键词: 不同盐度, 海洋真菌, 分子网络, 次生代谢产物, 生物活性

Abstract:

【Objective】 A marine fungus Aspergillus unguis DLEP2008001 was used for investigating the influence of salinity on the bioactivity and secondary metabolites. 【Method】 The crude extract samples of this strain cultured under different salinities in solid and liquid mediums for 14 and 28 days were analyzed by thin layer chromatography and antioxidative, acetylcholinesterase（AChE）inhibitory, and antimicrobial bioautographies to compare the bioactive secondary metabolites. The secondary metabolite diversity was further investigated by high performance liquid chromatography and “Multi-approach Assisted Feature Based Molecular Network（FBMN）” metabolomic analytical method based on liquid chromatography-tandem mass spectrometry（LC-MS/MS）. 【Result】 The salinity regulated the yield and diversity of antioxidant, AChE inhibitory ingredients and anti-microbial. In seawater-potato-sucrose liquid medium, the strain presented the most fertile feature metabolites when cultured for 28 d under salinity of 35 g/L, while in rice solid medium, it produced the most abundant predominant compounds under salinity of 5 g/L and 35 g/L as the second best condition. The average molecular weights of the predominant metabolites from solid culture generally deceased with the ascending of the salinity and they were mostly small molecules with multiple hydroxyl and amino groups, which are speculated to involve the adjustment of osmotic pressure. 【Conclusion】 Salinity exerts a significant influence on the bioactivity and secondary metabolites of this strain.

Key words: different salinities, marine fungi, molecular network, secondary metabolites, biological activity

康晓博, 张璟汐, 卢甜甜, 刘亚月, 周龙建, 张翼. 不同盐度培养下海洋真菌Aspergillus unguis DLEP2008001生物活性及次生代谢组变化[J]. 生物技术通报, 2024, 40(11): 296-311.

KANG Xiao-bo, ZHANG Jing-xi, LU Tian-tian, LIU Ya-yue, ZHOU Long-jian, ZHANG Yi. Variation of Bioactivities and Secondary Metabolomics of Marine Fungus Aspergillus unguis DLEP2008001 Cultured under Different Salinities[J]. Biotechnology Bulletin, 2024, 40(11): 296-311.

图/表 11

图1 菌株液体和固体培养第14天和第28天提取物薄层层析分析及抗氧化与乙酰胆碱酯酶抑制活性自显影结果 A1-A6：菌株提取物254 nm紫外图像； B1-B6：菌株提取物365 nm荧光图像；C1-C6：菌株提取物DPPH自由基清除活性自显影图像；D1-D6：菌株提取物AChE抑制活性自显影图像；E1-E6：菌株提取物茴香醛-浓硫酸显色图像；F1-F6：菌株提取物三氯化铁-铁氰化钾显色图像。图片下的数字表示盐度（单位：g/L），下同

Fig. 1 Thin layer chromatography analysis of extracts from the liquid culture and solid culture of the strain on the day 14 and 28 and bioautography images of anti-oxidative and acetylcholinesterase's inhibitory activity A1-A6: 254 nm UV images of strain extract; B1-B6: 365 nm fluorescence images of strain extract; C1-C6: bioautography images of DPPH radical scavenging activity; D1-D6: bioautography images of strain extract AChE inhibitory activity; E1-E6: colorized images of strain extract anisaldehyde-sulfuric acid; F1-F6: colorized images strain extract iron trichloride-potassium ferrocyanide. The number under the images indicate different salinities（unit: g/L）. The same below

表1 菌株不同组别提取物薄层层析分析及抗氧化与乙酰胆碱酯酶抑制活性自显影中的主要差异斑点及其盐度条件

Table 1 Main different spots displayed in the thin layer chromatography analysis and anti-oxidative and acetylcholinesterase inhibitory bioautographies of different groups of fungal extracts and corresponding salinity conditions

培养类型Culture type	培养时间Culture time/d	提取物 Extracts	不同手段展示的主要差异斑点（比移值）及其对应盐度 The main different spots（shown by R_fvalues）displayed by different approaches and the corresponding salinities
培养类型Culture type	培养时间Culture time/d	提取物 Extracts	254 nm紫外光 254 nm ultraviolet	365 nm紫外光 365 nm ultraviolet	抗氧化活性自显影 Antioxidant bioautography	AChE抑制活性自显影 AChE inhibitory bioautography	茴香醛显色 Anisaldehyde coloration	铁氰化钾-三氯化铁显色Potassium ferricyanide-FeCl₃ coloration
液体培养Liquid culture	14	菌丝体提取物 Mycelial extract	—	—	—	R_f（0.6, 0.8）: 10, 15 g/L	R_f（0.2, 1.0）: 2, 5, 10 g/L	—
	14	发酵液提取物 Broth extract	—	R_f（0.6, 1.0）: 5 g/L	R_f（0.4, 0.8）: 0.5, 2, 5 g/L	R_f（0.8, 1.0）: 0, 0.5, 2, 5 g/L	—	—
	28	菌丝体提取物 Mycelial extract	—	—	—	—	R_f（0.0, 1.0）: 5 g/L	—
	28	发酵液提取物 Broth extract	R_f（0.8, 1.0）: 0, 0.5 g/L	—	R_f（0.5）: 0, 0.5 g/L	—	—	—
固体培养Solid culture	14	总提取物 Total extract	R_f（0.4, 1.0）: 5, 10 g/L	—	R_f（0.4, 1.0）: 5, 10 g/L	R_f（0.4, 0.6）: 0, 0.5, 2 g/L R_f（0.6, 0.8）: 5, 10 g/L	R_f（0.0, 1.0）: 5 g/L	R_f（0.4, 1.0）: 5, 10 g/L
固体培养Solid culture	28	总提取物 Total extract	R_f（0.6, 1.0）: 5, 10 g/L	—	R_f（0.2, 0.5）: 5, 10 g/L	R_f（0.8, 1.0）: 5 g/L	R_f（0.0, 1.0）: 5 g/L	R_f（0.6, 0.8）: 5, 10 g/L R_f（0.2, 0.4）: 5 g/L

图2 菌株提取物抗菌活性初筛结果的代表性图片

Fig. 2 Representative images for the preliminary screening results of antibacterial activities of strain extracts

表2 不同盐度培养菌株提取物抗菌活性初筛结果

Table 2 Preliminary antimicrobial screening results of the extracts of the strain cultured under different salinities

培养方式及时间 Type and time of culture	盐度Salinity/（g·L^-1）	对不同指示菌的抗菌活性强度 Antimicrobial intensity to different indicator strains
培养方式及时间 Type and time of culture	盐度Salinity/（g·L^-1）	BS	SA	EC	PA	CA
液体培养14 d Liquid culture for 14 d	0	-	-	-	-	-
	0.5	-	-	-	-	-
	2	++	-	-	+	+
	5	+++	-	-	++	-
	10	+++	-	-	+	-
	15	-	-	-	-	-
	20	-	-	-	-	-
	35	-	-	-	-	-
液体培养28 d Liquid culture for 28 d	0	-	-	-	-	-
	0.5	-	-	-	-	-
	2	+++	-	-	+	-
	5	+++	-	-	++	-
	10	+++	-	-	+++	-
	15	-	-	-	-	-
	20	-	-	+	-	-
	35	-	-	+	-	-
固体培养14 d Solid culture for 14 d	0	+++	-	-	++	++
	0.5	+++	-	-	++	#
	2	-	-	-	++	#
	5	-	-	-	-	+
	10	-	-	-	-	+
	15	-	-	-	-	+++
	20	-	-	-	-	+++
	35	+++	-	-	++	++
固体培养28 d Solid culture for 28 d	0	+++	-	-	-	+++
	0.5	++	-	+	+	+++
	2	+++	-	+++	+++	++
	5	++	-	++	++	#
	10	+++	-	-	-	#
	15	-	-	-	-	#
	20	-	-	-	-	#
	35	-	-	-	-	+++

图3 菌株不同培养条件提取物抗菌活性层析自显影复筛结果 A1-A4：第14天液体培养提取物、第28天液体培养提取物、第14天固体培养提取物、第28天固体培养提取物抑制铜绿假单胞菌活性层析自显影结果；B1-B2：第28天液体培养提取物、第28天固体培养提取物抑制大肠杆菌活性层析自显影结果。C1-C4：第14天液体培养提取物、第28天液体培养提取物、第14天固体培养提取物、第28天固体培养提取物抑制枯草芽孢杆菌活性层析自显影结果。D1-D3：第14天液体培养提取物、第14天固体培养提取物、第28天固体培养提取物抑制白色假丝酵母活性层析自显影结果

Fig. 3 Bioautography re-screening results of the anti-microbial activities of the strain extracts via thin layer chromatography analysis A1-A4: The anti-Bacillus subtilis bioautography results of culture extracts of 14 d liquid culture, 28 d liquid culture, 14 d solid culture, and 28 d solid culture; B1-B2: the anti-Eschrichia coli bioautography results of culture extracts of 28 d liquid culture and 28 d solid culture; C1-C4: the anti-Pseudomonas aeruginosa bioautography results of culture extracts of 14 d liquid culture, 28 d liquid culture, 14 d solid culture, and 28 d solid culture; D1-D3: the anti-Candida albicans bioautography results of culture extracts of 14 d liquid culture, 14 d solid culture, and 28 d solid culture

图4 菌株不同盐度培养提取物的高效液相色谱分析（二极管阵列检测器检测的全波长等高线图）

Fig. 4 High performance liquid chromatography analysis of the strain extracts from different salinity cultures（The results are the full wavelength contour chromatograms detected by the diode array detector）

图5 菌株不同盐度液体和固体培养第28天提取物的液相色谱联用质谱分析

Fig. 5 Liquid chromatography-tandem mass spectrometry analysis of the strain extracts from different salinity liquid and solid cultures on day 28

图6 菌株液体培养基第28天提取物的分子网络图

Fig. 6 Molecular network diagram results of extracts of the strain on the 28th day of liquid culture medium

图7 菌株固体培养基第28天提取物的分子网络图

Fig. 7 Molecular network diagram of extract of the strain on the day 28 of solid culture medium

表3 液体和固体培养28天提取物中的盐度特征代谢产物的详细注释

Table 3 Detailed annotation of the salinity featured metabolites in the day 28 extracts of the liquid and solid medium cultures

培养类型Culture type	盐度 Salinity /（g·L^-1）	代谢物编号 No.of metabolite	离子质荷比Mass-to-charge ratio of the precursor ion（m/z）	缀合离子形式Form of adduct ions	分子式 Molecular formula	化合物名称 Compound name	已有报道真菌来源 Previously reported fungal origin	真菌来源文献 Literature for fungal origin
液体培养基 Liquid culture	0.5	化合物1 Compound 1	417.1435	[M+Na]⁺	C₂₁H₂₇ClO₅	Isochromophilones IV	Penicillium multicolor	[21]
液体培养基 Liquid culture	2	化合物2 Compound 2	477.3148	[M+H-H₂O]⁺	C₂₈H₄₆O₇	20-Hydroxyecdysone	Tapinella panuoides	[22]
固体培养基 Solid culture	5	化合物3 Compound 3	304.1362	[M+H]⁺	C₁₃H₂₁NO₇	麦角菌素类 Mycosporin	Gnomonia leptostyla	[23]
		化合物4 Compound 4	152.0088	[M+H]⁺	C₇H₅NOS	2-苯并噻唑酮 2- Benzothiazolone	Dipodascus sp.	[24]
		化合物5 Compound 5	233.1478	[M+H-H₂O]⁺	C₁₅H₂₂O₃	倍半萜类 Sesquiterpenoid	Drechslera gigantea	[25]
		化合物6 Compound 6	169.0424	[M+H]⁺	C₈H₈O₄	苔色酸 Orsellinic acid	Aspergillus sp.	[26-27]
		化合物7 Compound 7	237.1435	[M+H]⁺	C₁₄H₂₂O₄	Gliocladic acid	Trichoderma virens	[28]
	10	化合物8 Compound 8	277.0707	[M+H]⁺	C₁₄H₁₂O₆	Talaroflavone	Talaromyces flavus et al	[29-30]
	35	化合物9 Compound 9	214.0542	[M+H]⁺	C₆H₁₃N₃O₃	瓜氨酸 Citrulline	Schizosaccharomyces pombe	[31]
		化合物10 Compound 10	327.1181	[M+H]⁺	C₁₉H₁₈O₅	Unguinol	Aspergillus unguis	[12,32]
		化合物11 Compound 11	380.1190	[M+H]⁺	C₁₃H₂₁N₃O₈S	S-D-乳酰谷胱甘肽 S-Lactoylglutathione	Saccharomyces cerevisiae	[33]

图8 菌株液体和固体培养不同盐度下优势代谢产物的前体离子质荷比分布

Fig. 8 Distribution of precursor m/z values of the predominant metabolites for the liquid and solid cultures of the strain under different salinities

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不同盐度培养下海洋真菌Aspergillus unguis DLEP2008001生物活性及次生代谢组变化

Variation of Bioactivities and Secondary Metabolomics of Marine Fungus Aspergillus unguis DLEP2008001 Cultured under Different Salinities

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