灵芝Ganoderma lingzhi S.H. Wu, Y. Cao & Y.C. Dai过去被误认为Ganoderma lucidum (Curtis) P. Karst，别名赤芝、木灵芝和灵芝草，古称“瑞草”(戴玉成等 2013, 2021)，是我国医药宝库中的一颗璀璨明珠，早在两千多年前就开始采集利用，古籍中记载灵芝具有延年益寿、扶正固本及滋补身体等多种功效(Zhou et al. 2012；Wu et al. 2019)，在中国、东北亚和东南亚地区得到广泛使用。现代药理学研究表明，灵芝具有降血糖、抗肿瘤、保肝及延缓衰老等药理作用(Yang et al. 2019)，已被收录到《中华人民共和国药典》以及《美国草药药典与治疗概要》中(Wang & Ng 2006)。灵芝对人类健康的作用也日益受到国内外专家的重视，进一步解析和开发灵芝的药理作用是当前国内外研究的一个热点。
然而灵芝以及其他真菌中脂质组分的相关研究还鲜有报道，主要原因是脂质种类繁多、结构复杂且含量差异大，传统的薄层色谱和气相色谱技术难以达到有效的分离与鉴定(吴邦富等 2018)。随着脂质组学技术发展和不断完善，脂质组学已被广泛应用于脂质构成鉴定、疾病诊断、药物靶点及先导化合物的发现等方面(陆姝欢等 2007)。章丽等(2021)运用超高效液相色谱-四极杆/静电场轨道阱高分辨质谱分析了在正负离子模式下嗜热链球菌发酵乳中脂质的构成；谢宏宇(2016)等通过对卵巢癌患者和对照患者的血液脂质组学数据进行分析，筛选出可作为诊断卵巢癌生物标志物的8个差异脂质；Sewell et al. (2012)通过质谱分析法和稳定同位素标记法分析了巨噬细胞鞘脂类和磷脂类成分，探究了脂质构成对克罗恩病的影响。
本研究基于超高效液相色谱-电喷雾串联四极杆法(ultra-high-performance liquid chromatography electrospray ionization tandem mass spectrometry, UPLC-ESI-MS/MS)技术，鉴定了灵芝细胞中甘油酯、磷脂、鞘脂和固醇4类脂质，以及游离脂肪酸成分的组成和占比，系统性分析了灵芝细胞脂质组分，为后续灵芝中脂质有效成分的研究奠定基础。
1 材料与方法
1.1 材料、试剂和主要仪器
1.1.1 菌种
灵芝CGMCC 18819，购于中国普通微生物菌种保藏管理中心。
1.1.2 培养基
斜面培养基(g/L)：马铃薯200，葡萄糖10，琼脂粉20，硫酸镁1.5，磷酸二氢钾3.0，VB1 0.05。种子培养基(g/L)：葡萄糖35，蛋白胨5，酵母膏2.5，磷酸二氢钾1，硫酸镁0.5，VB1 0.05，玉米粉5。发酵培养基(g/L)：蛋白胨5.6，葡萄糖38，磷酸氢二钾1.53，VB1 0.05，初始pH 7.0。
1.1.3 试剂
乙腈(色谱纯)，Fisher公司；异丙醇，乙酸，甲酸铵，葡萄糖，琼脂粉，硫酸镁，磷酸二氢钾，VB1，酵母膏，蛋白胨(均为优级纯)。
1.1.4 仪器和设备
超高效液相色谱(ultra performance liquid chromatography，UPLC; Shim-pack UFLC SHIMADZU CBM30A，
1.2 灵芝发酵培养
灵芝斜面菌种接种至种子培养基中，28 ℃、160 r/min黑暗培养7 d，以10%接种量转接至发酵培养基(装液量100 mL/250 mL三角瓶)，25.8 ℃、146 r/min黑暗培养7 d，获得灵芝菌丝体样品。
1.3 脂质成分提取
灵芝菌丝体样品采用冷冻干燥仪进行冷冻干燥后研磨，称量粉末50 mg，加入1 mL异丙醇涡旋混匀，4 ℃超声提取10 min。4 ℃、12 000 r/min离心10 min，取上清液800 μL低温浓缩干燥，加入200 μL异丙醇复溶后用于液相色谱质谱检测分析。
1.4 色谱质谱条件
色谱条件：Accucore C30色谱柱(2.1 mm× 100 mm，2.6 μm)，柱温40 ℃；流速0.35 mL/min；进样量3 μL。流动相A：水-乙腈(40:60，体积比)，含10 mmol/L甲酸铵和0.04%乙酸；流动相B：异丙醇-乙腈(90:10，体积比)，含10 mmol/L甲酸铵和0.04%乙酸；梯度洗脱条件：0-2 min，80% A，20% B；2-4 min，70% A，30% B；4-9 min，35% A，65% B；9-14 min，15% A，85% B；14-15.5 min，10% A，90% B；15.5-17.7 min，5% A，95% B；17.7-20 min，80% A，20% B。
质谱条件：电喷雾离子源(electrospray ionization，ESI)温度550 ℃，质谱电压5 500 V (positive)，−4 500 V (negative)，离子源气体Ⅰ(GS Ⅰ) 55 psi，气体Ⅱ(GS Ⅱ) 60 psi，气帘气(curtain gas，CUR) 25 psi，碰撞诱导电离(collision-activated dissociation, CAD)参数设置为高。在三重四极杆(Qtrap)中，每个离子对是根据优化的去簇电压(declustering potential, DP)和碰撞能(collision energy, CE)进行扫描检测。采集范围为m/z 120-1 800，正负离子同时采集；一级质谱分辨率为70 000，二级质谱分辨率为17 500。
1.5 数据分析
使用Lipid Search软件，读取LC-MS/MS导出的raw格式原始数据，根据样本中的母离子和多级质谱数据，鉴定其中脂质分子结构及其正负离子的加合模式；物质相对含量根据色谱峰面积获得。本研究脂质组学鉴定与武汉康之代谢生物科技有限公司合作完成。
2 结果与分析
2.1 灵芝中脂质成分概述
采用UPLC-ESI-MS/MS对灵芝中脂质组分进行分析，在正、负离子模式下检测到的脂质组分见附表1、附表2 (国家微生物科学数据中心NMDCX0000166)，正离子模式下检测到脂质成分共计225种，在负离子模式下检测到脂质成分71种。
统计鉴定结果表明，灵芝细胞中含有甘油酯、磷脂、鞘脂和甾醇4大类脂质。其中甘油酯占总脂质含量最多，为44.70%，磷脂和鞘脂分别为38.06%和17.08%，甾醇占比最少，为0.16% (图1)。
图1
图1
灵芝细胞中主要脂质成分占比情况
Fig. 1
Proportion of main lipid components in Ganoderma lingzhi cells.
2.2 灵芝中甘油酯的成分构成
甘油酯均在正离子模式下被检测(附表1，国家微生物科学数据中心NMDCX0000166)，主要含有甘油三酯(triacylglycerol, TG)、甘油二酯(diacylglycerol, DG)和单甘油酯(monoglyceride, MG)类，TG为灵芝细胞中最主要的甘油酯，TG、DG和MG的相对含量分别为67.36%、31.87%和0.77% (图2A)，其中TG共鉴定到75种、DG共鉴定到31种，MG共鉴定到6种(附表1，国家微生物科学数据中心NMDCX0000166)。
图2
图2
灵芝细胞中甘油酯质占比情况
A：甘油酯主要成分占比. B：甘油三酯亚成分占比. C：甘油二酯亚成分占比. D：单甘油酯亚成分占比
Fig. 2
Proportion of glycerolipid content in Ganoderma lingzhi cells.
A: The proportion of the main components in triglyceride. B: The proportion of TG subcomponents. C: The proportion of DG subcomponents. D: The proportion of MG subcomponents.
TG亚成分分析表明，TG (16:0/18:2/20:4)、TG (18:1/18:2/18:2)、TG (18:1/18:1/18:2)、TG (16:1/18:2/18:2)和TG (16:0/18:2/18:2)占总TG含量较多，分别为15.06%、11.77%、10.97%、9.98%和7.62% (图2B)。
在灵芝细胞中共检测到的31种DG亚成分，其中DG (18:2/18:2)、DG (16:0/18:2)、DG (16:1/18:2)、DG (18:0/18:2)和DG (16:0/16:0)占总DG含量较多，分别为28.20%、17.20%、15.26%、9.26%和7.40% (图2C)。
分析MG亚成分发现，MG (16:0)和MG (18:0)占总MG含量较多，分别为MG总含量的57.48%和37.94% (图2D)。
2.3 灵芝中磷脂的成分构成
灵芝细胞中检测到的磷脂可分为溶血型磷脂(lysophospholipid，也称L型磷脂)和非溶血型磷脂(non-lysophospholipid)，其中溶血型磷脂的相对含量占磷脂总量的16.90%，非溶血型磷脂的相对含量占磷脂总量的83.10% (图3A)。
图3
图3
灵芝细胞中磷脂占比情况
A：溶血磷脂与非溶血磷脂占比. B：溶血磷脂主要成分占比. C：非溶血磷脂主要成分占比. D：PE亚成分占比. E：PA亚成分占比. F：PC亚成分占比. G：PG亚成分占比. H：PI亚成分占比. I：PS亚成分占比
Fig. 3
Proportion of phospholipid content in Ganoderma lingzhi cells.
A: The ratio of lysophospholipid and non-lysophospholipid. B: The proportion of the main components in lysophospholipid. C: The proportion of the main components in non-lysophospholipid. D: The proportion of PE subcomponents. E: The proportion of PA subcomponents. F: The proportion of PC subcomponents. G: The proportion of PG subcomponents. H: The proportion of PI subcomponents. I: The proportion of PS subcomponents.
2.3.1 灵芝中溶血型磷脂的成分构成
灵芝细胞中共检测到的6类L型磷脂，占比较多的为溶血磷脂酸(lysophosphatidic acid, LPA)、溶血磷脂酰乙醇胺(lysophosphatidylethanolamine, LPE)和溶血磷脂酰胆碱(lysophosphatidylcholines, LPC)分别占总溶血型磷脂含量的52.27%、38.08%和5.47%，此外，在灵芝细胞中还检测到少量溶血磷脂酰甘油(lysophosphatidylglycerol, LPG)、溶血磷脂酰肌醇(lysophosphatidylinositol, LPI)和溶血磷脂酰丝氨酸(lysophosphatidylserine, LPS)，占总溶血型磷脂含量之和为4.18% (图3B)。
2.3.2 灵芝中非溶血型磷脂的成分构成
灵芝细胞中共检测到的6类非溶血型磷脂，占比较多的为磷脂酰乙醇胺(phosphatidylethanolamine, PE)、磷脂酸(phosphatidic acid, PA)和磷脂酰胆碱(phosphatidylcholine, PC)，分别占总非溶血型磷脂含量的62.64%、18.14%和10.68%；其他3类非溶血型磷脂为磷脂酰丝氨酸(phosphatidylserine, PS)、磷脂酰肌醇(phosphoinositides, PI)和磷脂酰甘油(phosphatidylglycerol, PG)，共计占总非溶血型磷脂含量的8.54% (图3C)。
进一步分析6类非溶血型磷脂亚成分发现，灵芝细胞中共含有30种PE种类(附表1、附表2，国家微生物科学数据中心NMDCX0000166)，其中PE (18:1/16:1)、PE (18:2/18:2)、PE (16:0/18:1)、PE (16:1/18:2)和PE (18:2/14:0)占比较高，分别占总PE含量的41.52%、24.31%、13.04%、9.62%和3.36% (图3D)。
从灵芝细胞中共检测出10种PA亚成分(附表1，国家微生物科学数据中心NMDCX0000166)，其中PA (18:2/18:2)和PA (16:0/18:2)占比较高，分别占PA含量的58.81%和40.34% (图3E)。
在灵芝样品中共检测出30种PC亚成分(附表1、附表2，国家微生物科学数据中心NMDCX0000166)，其中PC (16:0/18:3)相对含量最多，为47.17%，其余含量较高的成分为PC (14:0/18:2)、PC (18:1/24:1)、PC (18:2/18:2)和PC (16:0/20:5)，其相对含量分别为12.23%、8.46%、6.01%和5.90% (图3F)。
2.4 灵芝中鞘脂的成分构成
灵芝细胞中检测到鞘脂成分为神经酰胺(ceramide, Cer)、鞘磷脂(sphingomyelin, SM)、鞘氨醇(sphingosine, Sph)和糖鞘脂(glycosphingolipids, GSL)，Cer和SM相对含量较多，分别为60.33%和31.49%，Sph和GSL相对含量较少，分别为7.25%和 0.93% (图4A)。
图4
图4
灵芝细胞中鞘脂含量占比情况
A：鞘脂主要成分占比. B：神经酰胺亚成分占比. C：鞘磷脂亚成分占比. D：鞘氨醇亚成分占比. E：糖鞘脂亚成分占比
Fig. 4
Proportion of sphingolipids in Ganoderma lingzhi cells.
A: The proportion of the main components in sphingolipids. B: The proportion of Cer subcomponents. C: The proportion of SM subcomponents. D: The proportion of Sph subcomponents. E: The proportion of GSL subcomponents.
分析鞘脂亚成分发现，灵芝中共检测出19种Cer亚成分、7种SM亚成分、3种Sph亚成分和5种GSL亚成分(附表2，国家微生物科学数据中心NMDCX0000166)。
Cer亚成分中Cer (d18:1/16:1)、Cer (d18:0/ 18:0)、Cer (d18:0/16:0)、Cer (d18:1/18:0)和Cer (d18:1/16:0)含量较高，其相对含量分别为30.34%、21.48%、20.51%、10.08%和9.06%。其余检测到一些含量较少的神经酰胺亚成分，相对含量之和为8.53% (图4B)。
2.5 灵芝中脂质成分的游离脂肪酸构成
本研究共检测出27种游离脂肪酸(附表3，国家微生物科学数据中心NMDCX0000166)，其中20种为不饱和脂肪酸(unsaturated fatty acids, UFA)，相对含量为65.59%；7种为饱和脂肪酸(saturated fatty acids, SFA)，相对含量为34.41% (图5A)。在饱和脂肪酸中，占比较多的为棕榈酸(16:0)、硬脂酸(18:0)、花生酸(20:0)和二十四烷酸(24:0)，其占比分别为50.33%、16.24%、13.25%和12.23% (图5B)。在不饱和脂肪酸中，占比较多的为亚油酸(18:2)、油酸(18:1)和棕榈油酸(16:1)，其相对含量分别为34.40%、24.47%和15.05% (图5C)。
图5
图5
灵芝细胞中脂肪酸占比情况
A：饱和脂肪酸和不饱和脂肪酸占比. B：饱和脂肪酸亚成分占比. C：不饱和脂肪酸亚成分占比
Fig. 5
Proportion of fatty acid in Ganoderma lingzhi cells.
A: The ratio of UFA and SFA. B: The proportion of SFA subcomponents. C: The proportion of UFA subcomponents.
3 讨论
脂质是人类主要营养成分，食药用真菌是人类摄取脂质营养的重要来源之一，但在名贵的食药用真菌灵芝中开展脂质成分鉴定研究还鲜有报道。本研究采用UPLC-ESI-MS/MS技术，对灵芝细胞中的脂质构成进行了系统性鉴定与分析，结果共鉴定到296种脂质，其中甘油酯112种，磷脂148种，鞘脂34种，甾醇2种，以及游离脂肪酸27种，为灵芝的营养功能和脂质代谢后续相关研究奠定基础。
甘油酯在动物细胞中具有多种生理活性和营养功能。在人体中，中碳链脂肪酸TG可通过改善胰岛素的分泌来调节血液中葡萄糖的含量，长碳链脂肪酸TG则最终将转变为脂肪组织储存于体内，以供能量的需要(Han et al. 2007)；在大鼠中，中碳链膳食DG可以降低血清中的TG，抑制脂类物质在主动脉膜上的堆积，具有预防和治疗脂肪肝的作用，对治疗动脉粥样硬化也有一定疗效(Hara et al. 1993)。本研究发现，灵芝细胞中，中碳链脂肪酸TG (16:10/18:2/20:4)、TG (18:1/18:2/18:2)和TG (18:1/18:1/18:2)占总灵芝TG含量较多，暗示灵芝在改善胰岛素分泌方面具有潜力。中碳链脂肪酸DG (18:2/18:2)、DG (16:0/18:2)、DG (16:1/18:2)和DG (18:0/18:2)占总灵芝DG含量较多，暗示灵芝在预防脂肪肝和动脉粥样硬化等疾病方面具有潜力。
目前在双孢蘑菇、平菇和金针菇等食药用真菌中，已初步开展了脂质成分鉴定研究，但鉴定类别上主要集中在脂肪酸类别上，缺乏全面系统的脂质成分分析。在双孢蘑菇中，采用了气相色谱方法发现，双孢蘑菇中所含不饱和脂肪酸居多，主要为亚油酸(18:2) (Necmettin et al. 2006)。在平菇中，采用气相色谱方法，鉴定到不饱和脂肪酸居多，最主要的脂肪酸成分为油酸(18:1)和亚油酸(18:2) (Cohen et al. 2014)。在金针菇中，通过气相色谱串联质联方法，鉴定到不饱和脂肪酸居多，主要的脂肪酸成分为亚油酸(18:2) (Kwang et al. 2011)。本研究鉴定到灵芝中游离的不饱和脂肪酸多于饱和脂肪酸，且主要脂质成分为亚油酸(18:2)和油酸(18:1)，体现了食药用菌脂肪酸比例的一致性。并且，不同食药用菌的脂肪酸成分分析结果表明，食用菌总脂肪含量的特点是不饱和脂肪酸比例高，大多数情况下以亚油酸和油酸为主(Sande et al. 2019)。
脂肪酸是多种脂质的结构单元，脂肪酸的长度以及不饱和度，会导致脂质功能的差异(Burdge & Calder 2015)。长期摄入过量饱和脂肪酸会产生凝血、炎症和胰岛素抵抗等不良影响(Eguchi et al. 2012)，尤其是月桂酸(12:0)、肉豆蔻酸(14:0)和棕榈酸(16:0)等，会增加心血管疾病、冠心病和Ⅱ型糖尿病的风险(Chowdhury et al. 2014)。相比于饱和脂肪酸，不饱和脂肪酸被认为是更加健康的。摄入不饱和脂肪酸可以降低血液胆固醇、调节细胞生理活动和显著降低冠心病的患病率(Hossain et al. 2003；Jakobsen et al. 2009)。本研究发现，在灵芝细胞中，不饱和脂肪酸占总脂肪酸的65.59%，表明灵芝脂质成分对人体健康有益。
本研究基于脂质组学对灵芝胞内脂质成分进行系统性分析，对于全面解析灵芝脂质构成、挖掘灵芝的药用价值和功能特性具有重要指导意义，也可为灵芝的利用以及新型药品的开发提供参考。
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