Filamentous phage SW1 is active and influences the transcriptome of the host at high‐pressure and low‐temperature

Abstract

As the most abundant biological entities on the planet, viruses are involved in global biogeochemical cycles, and they have been shown to play an important role in the overall functioning of the deep-sea ecosystem. Nevertheless, little is known about whether and how deep-sea viruses affect the physiology of their bacterial hosts. Previously, the filamentous phage SW1 was identified in the bathypelagic bacterium Shewanella piezotolerans WP3, which was isolated from the upper sediment of West Pacific ocean. In this study, phage SW1 was shown to be active under in situ environmental conditions (20 MPa and 4°C) by transmission electron microscopy and reverse-transcription quantitative polymerase chain reaction. Further comparative analysis showed that SW1 had a significant influence on the growth and transcriptome of its host. The transcription of genes responsible for basic cellular activities, including the transcriptional/translational apparatus, arginine synthesis, purine metabolism and the flagellar motor, were down-regulated by the phage. Our results present the first characterization of a phage-host interaction under high-pressure and low-temperature conditions, which indicated that the phage adjusted the energy utilization strategy of the host for improved survival in deep-sea environments.

Lysogeny in the oceans: Lessons from cultivated model systems and a reanalysis of its prevalence

“…When grown on agar plates at ambient atmospheric pressure, S. piezotolerans strains infected by SW1 exhibited increased production of lateral flagella and enhanced swarming motility (Jian et al ., 2013). However, lateral flagella production was unaffected at high pressure (20 MPa) and phage‐cured strains exhibited higher growth rates (Jian et al ., 2016). Similar alterations to host gene expression and fitness have been seen with Pseudoalteromonas phage f327; it is anticipated this filamentous phage impairs host growth rate, cell density, and host tolerance to osmotic shock and reactive oxygen species (e.g., NaCl and H 2 O 2 ; Yu et al ., 2015).…”

A Genome-Scale Model of Shewanella piezotolerans Simulates Mechanisms of Metabolic Diversity and Energy Conservation

“…These studies provide a broad knowledge base for constructing the WP3 GEM. Furthermore, WP3 has established protocols for genetic manipulations (37–40). The experimental accessibility of this organism would enable the verification of modeling outcomes and support future research on molecular adaptations through combined GEM simulation and experimental verification.…”

Characteristics and ecological functions of deep-sea viruses

“…与模式丝状噬菌体 CTXΦ不同, SW1具有独特的操纵子构成且具有5′UTR 介导的基因表达调控方式 [55] . 此外, 定量PCR和电子显 微镜观察的结果表明SW1在高压低温条件下处于活跃 状态, 这也与其宿主来源的深海环境特征相吻合 [56] . 另 一株从深海沉积物中分离的噬菌体为BVW1, 其可侵染 Bacillus sp.…”

“…. 值得注意的是, 尽管目前在侵染自养微生物如 硫 氧 化 细 菌 的 深 海 病 毒 中 发 现 了 与 硫 代 谢 相 关 的 AMGs [70] , [56,75] . 我们首先构建了完全不含噬菌体SW1的WP3 菌株WP3ΔSW1, 经过基因芯片对比分析, 发现侧生鞭 毛基因簇的15个基因在WP3ΔSW1中都显著下调 [75] .…”

“…对翻译的影响主要表现在一些编 码核糖体亚基蛋白的基因(rplO, rplR, rpsK, rpsH, rplQ, rpsE, rpsM), 以及编码核糖体结合因子(rbfA), rRNA甲 基化酶(rlmB), 尿嘧啶合成酶(rsuA)的基因转录水平上 调, 程度在2~4倍之间 [56] . 反过来也说明了在深海环境 中, WP3被丝状噬菌体SW1侵染后, 会下调其转录和翻 译元件的合成, 从而降低能量消耗 [56] . [15,81] .…”