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Diversity and Co-Occurrence Patterns of Soil Bacterial and Fungal microorganisms Article Diversity and Co-Occurrence Patterns of Soil Bacterial and Fungal Communities of Chinese Cordyceps Habitats at Shergyla Mountain, Tibet: Implications for the Occurrence 1, 1, 1 1 2 1 Jun-Li Shao y, Bei Lai y, Wei Jiang , Jia-Ting Wang , Yue-Hui Hong , Fu-Bin Chen , Shao-Qing Tan 1 and Lian-Xian Guo 1,* 1 Dongguan Key Laboratory of Environmental Medicine, School of Public Health, Guangdong Medical University, Dongguan 523808, China 2 Department of Basic Medicine, Guangdong Jiangmen Chinese Medical College, Jiangmen 529000, China * Correspondence: [email protected]; Tel.: +86-0769-22896573 These authors contributed equally to this work. y Received: 12 July 2019; Accepted: 20 August 2019; Published: 22 August 2019 Abstract: Chinese Cordyceps is a well-known medicinal larva-fungus symbiote distributed in the Qinghai-Tibetan Plateau and adjacent areas. Previous studies have involved its artificial cultivation but commercial cultivation is difficult to perform because the crucial factors triggering the occurrence of Chinese Cordyceps are not quite clear. The occurrence of Chinese Cordyceps is greatly affected by the soil environment, including the soil’s physicochemical and microecological properties. In this study, the effects of these soil properties on the occurrence of Chinese Cordyceps were investigated. The results show that the physicochemical properties, including easily oxidizable organic carbon (EOC), soil organic carbon (SOC), humic acid carbon (HAC), humin carbon (HMC), and pH, might be negatively related to the occurrence of Chinese Cordyceps, and soil water content (SWC) might be positively related. Several soil physicochemical parameters (pH, SOC, HMC, HAC, available potassium (APO), available phosphorus (APH), microbial biomass carbon (MBC), and the ratio of + + NH4 to NO3− (NH4 /NO3−)) and microbial properties interact and mix together, which might affect the occurrence of Chinese Cordyceps. Soil microbial community structure was also a possible factor, and a low level of bacterial and fungal diversity was suitable for the occurrence of Chinese Cordyceps. The intra-kingdom network revealed that a closer correlation of the bacterial community might help the occurrence of Chinese Cordyceps, while a closer correlation of the fungal community might suppress it. The inter-kingdom network revealed that the occurrence rate of Chinese Cordyceps might be negatively correlated with the stability of the correlation state of the soil habitat. In conclusion, this study shows that soil physicochemical properties and microbial communities could be greatly related with the occurrence of Chinese Cordyceps. In addition, soil physicochemical properties, the level of bacterial and fungal diversity, and correlations of bacterial and fungal communities should be controlled to a certain level to increase the production of Chinese Cordyceps in artificial cultivation. Keywords: Chinese Cordyceps; Ophiocordyceps sinensis; soil physicochemical properties; bacterial community; fungal community; co-occurrence analysis 1. Introduction Ophiocordyceps sinensis, also known as Cordyceps sinensis, is a well-known symbiote of fungus (O. sinensis) and larva (Thitarodes, Hepialidae, Lepidoptera)[1]. It is particularly distributed in the Qinghai-Tibetan Plateau and adjacent high-altitude areas [2] and is usually called Chinese Cordyceps for Microorganisms 2019, 7, 284; doi:10.3390/microorganisms7090284 www.mdpi.com/journal/microorganisms Microorganisms 2019, 7, 284 2 of 21 Microorganisms 2019, 7, 284 2 of 23 forthe the fungus-larva fungus-larva symbiote. symbiote.In this In paper, this paper, in order in to order avoid to misunderstanding, avoid misunderstanding, we use Chinese we useCordyceps Chineseto Cordycepsrefer to the to fungus-larva refer to the symbiote fungus-larva and O. sinensissymbioteto refer and to O. the sinensis fungus. to Chinese refer Cordycepsto the fungus.is an important Chinese Cordycepstraditional Chineseis an important medicine thattraditional can efficiently Chinese treat medicine cancer, hyperglycemia, that can efficiently hypertension, treat and cancer, other hyperglycemia,diseases [3]. These hypertension, medicinal functions and other create diseases a large [3]. demand These for medicinal wild Chinese functionsCordyceps create[4], a but large the demandyield is extremely for wild Chinese limited dueCordyceps to its complicated [4], but the lifeyield cycle is extremely [5], obligate limited parasitism, due to and its complicated ecogeographical life cyclepreference [5], obligate [6]. Worse parasi still,tism, the yield and ofecogeographical wild Chinese Cordyceps preferencesharply [6]. decreasedWorse still, in recentthe yield years of due wild to Chineseexcessive Cordyceps excavation, sharply habitat decreased destruction, in recent and years global due warming to excessive [7]. Theexcavation, serious imbalancehabitat destruction, between anddemand global and warming supply leads[7]. The to soaringserious retailimbalance prices between [8]. For decades,demand increasingand supply studies leads haveto soaring focused retail on pricesartificial [8]. cultivation For decades, on aincreasing large scale, studies but it hashave not focused been widely on artificial implemented cultivation due toon many a large unanswered scale, but itquestions has not regardingbeen widely the implemented mechanism of due occurrence to many (formation unanswered of the questions fungus-larva regarding symbiote) the mechanism on the host ofinsects occurrence [3,9]. (formation of the fungus-larva symbiote) on the host insects [3,9]. The infection of host Thitarodes larvae mainly occurs in soils (Figure1 1).). Thitarodes liveslives in in soil during its larvallarval stagestage (about (about 3 3 years) years) and and pupal pupal stage stage (40 (40 days) days) [3]. [3]. The The fungal fungal spores spores of O. of sinensis O. sinensisthat thaterupt erupt from from the mature the mature stroma stroma of Chinese of ChineseCordyceps Cordycepsrandomly randomly scatter inscatter topsoils, in topsoils, gradually gradually infiltrate infiltrateinto deeper into soils deeper by the soils delivery by the of delivery rainfall, developof rainfall, into develop infective into conidia, infective and conidia, enter into and the enterThitarodes into thelarvae Thitarodes [9]. However, larvae increasing[9]. However, research increasing has proved research that has the proved presence that of O.the sinensis presencemight of O. not sinensis be the mightcrucial not factor be the in the crucial occurrence factor in of Chinesethe occurrenceCordyceps of .Chinese For instance, Cordyceps the inoculation. For instance, of O. the sinensis inoculationthrough of O.spraying, sinensis feeding, through and spraying, injection feeding, could not and increase injection the occurrencecould not increase of Chinese theCordyceps occurrencevery of much Chinese [10]. CordycepsPrevious reportsvery much have [10]. also Previous shown that reportsO. sinensis have existedalso shown not only that inO. healthy sinensisThitarodes existed notlarvae, only but in healthyalso in the Thitarodes egg, pupa, larvae, and adult.but also In addition,in the egg, several pupa, studies and adult. have reportedIn addition, that several the synergistic studies ehaveffect reportedof different that fungi the synergistic might help effect to produce of different Chinese fungiCordyceps might help[9,11 to], indicatingproduce Chinese that the Cordyceps other microbial [9,11], indicatingfactors might that also the beother related microbial to its occurrence. factors might Field also investigations be related to revealedits occurrence. that although Field investigations the presence revealedof Chinese thatCordyceps althoughand the the presence host insect of areChinese characterized Cordyceps by and a very theclear host zonalinsect and arevertical characterized distribution by a verypattern clear [12 ],zonal the occurrenceand vertical rates distri (ratiobution of the pattern number [12], of the Chinese occurrenceCordyceps ratesto the(ratio number of the of numberThitarodes of Chineselarvae) show Cordyceps differences to the withinnumber the of sameThitarodes region larvae) [13]. These show discoveriesdifferences indicatedwithin the that same the region occurrence [13]. Theseof Chinese discoveriesCordyceps indicatedmight bethat influenced the occurrence by specific of Chinese environmental Cordyceps factors, might be especially influenced soil by factors. specific environmental factors, especially soil factors. Figure 1. LifeLife history history of of OphiocordycepsOphiocordyceps sinensis sinensis andand Thitarodes host [5]. [5]. The germination and and growth growth of of a a fungus fungus can can be suppressed by natural soils to to a a certain certain extent, extent, and this phenomenon isis referredreferred to to as as soil soil fungistasis fungistasis [14 [14].]. The The intensity intensity of of fungistasis fungistasis is dependentis dependent on onthe the soil soil physical physical and and chemical chemical properties properties as wellas we asll microbial as microbial activity activity [15, 16[15,16].]. Among Among them, them, the soilthe soilmicrobial microbial community community and activityand activity are influenced are influenced by the by physicochemical the physicochemical characteristics characteristics [17], and [17], in andturn, in the turn, soil the microbiome soil microbiome also plays also an plays important an impo rolertant in biogeochemical role in biogeochemical processes, processes,
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