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悄然发生:臭虫对昆虫病原体、环境细菌和人类病原体的转录组反应。

Under the radar: Transcriptomic responses of bed bugs to an entomopathogen, environmental bacteria, and a human pathogen.

机构信息

Department of Biochemistry, Nutrition, and Health Promotion, Mississippi State University, Mississippi State, MS, USA.

Department of Biochemistry, Molecular Biology, Entomology, and Plant Pathology, Mississippi State University, Mississippi State, MS, USA.

出版信息

J Invertebr Pathol. 2024 Sep;206:108182. doi: 10.1016/j.jip.2024.108182. Epub 2024 Aug 22.

DOI:10.1016/j.jip.2024.108182
PMID:39178984
Abstract

Bed bugs (Hemiptera: Cimicidae) are widely distributed, obligately blood-feeding insects, but they have never been linked to pathogen transmission in humans. Most other hematophagous insects that frequently bite humans transmit pathogens, and it is unclear why bed bugs do not. One hypothesis is that bed bugs have evolved a highly robust immune system because their mating system, traumatic insemination, exposes females to consistent wounding and bacterial infections. Although this has been proposed, very little is known about the bed bug immune system and how bed bugs respond to microbial challenges introduced by wounding. Similarly, there is little known about how the bed bug immune system responds to human pathogens. Understanding the bed bug immune system could give insight to why bed bugs appear not to transmit disease and under what circumstances they could, while also facilitating biological control efforts involving microbes. To investigate the transcriptomic response of bed bugs to immune challenges, we exposed female bed bugs to three bacterial challenges. 1.) Pseudomonas fluorescens, an entomopathogen known to have harmful effects to bed bugs, 2.) bacteria cultured from a bed bug enclosure (99.9 % Bacillus spp.), likely encountered during traumatic insemination, and 3.) Borrelia duttoni, a human vector-borne pathogen that causes relapsing fever. We compared the transcriptomes of infected bed bugs with uninfected matched controls in a pairwise fashion, focusing on immune-related genes. We found many known antimicrobial effector genes upregulated in response to P. fluorescens and traumatic insemination-associated bacteria, but interestingly, not in response to B. duttoni. In the differentially expressed genes that were shared between experiments, we found significant overlap in the P. fluorescens treatment and the traumatic insemination bacteria treatment, and between the P. fluorescens and B. duttoni treatments, but not between the traumatic insemination bacteria treatment and the B. duttoni treatment. Finally, we identify previously overlooked candidates for future studies of immune function in bed bugs, including a peroxidase-like gene, many putative cuticle-associated genes, a laccase-like gene, and a mucin-like gene. By taking a comprehensive transcriptomic approach, our study is an important step in understanding how bed bugs respond to diverse immune challenges.

摘要

臭虫(半翅目:臭虫科)广泛分布,是专性吸血昆虫,但它们从未与人类病原体传播有关。大多数其他经常叮咬人类的吸血昆虫会传播病原体,而臭虫为什么不传播病原体还不清楚。一种假设是,臭虫已经进化出了非常强大的免疫系统,因为它们的交配系统,创伤性授精,使雌性不断受到创伤和细菌感染。尽管这已经被提出,但人们对臭虫的免疫系统知之甚少,也不知道臭虫如何应对创伤带来的微生物挑战。同样,人们对臭虫的免疫系统如何应对人类病原体也知之甚少。了解臭虫的免疫系统可以深入了解为什么臭虫似乎不会传播疾病,以及在什么情况下它们可能会传播疾病,同时也有助于涉及微生物的生物控制工作。为了研究臭虫对免疫挑战的转录组反应,我们将雌性臭虫暴露于三种细菌挑战中。1. 荧光假单胞菌,一种对臭虫有有害影响的昆虫病原体,2. 从臭虫围场培养的细菌(99.9%的芽孢杆菌属),可能在创伤性授精期间遇到,3. 伯氏疏螺旋体,一种引起回归热的人类载体传播病原体。我们以配对的方式比较了感染臭虫与未感染匹配对照的转录组,重点关注与免疫相关的基因。我们发现许多已知的抗菌效应基因在响应 P. fluorescens 和创伤性授精相关细菌时上调,但有趣的是,它们没有响应 B. duttoni。在实验之间共享的差异表达基因中,我们发现 P. fluorescens 处理和创伤性授精细菌处理之间、P. fluorescens 和 B. duttoni 处理之间存在显著重叠,但创伤性授精细菌处理和 B. duttoni 处理之间没有重叠。最后,我们确定了以前被忽视的臭虫免疫功能研究的候选基因,包括过氧化物酶样基因、许多假定的角质层相关基因、漆酶样基因和粘蛋白样基因。通过采用全面的转录组学方法,我们的研究是了解臭虫如何应对各种免疫挑战的重要一步。

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