Prophage-encoded chitinase gene supports growth of its bacterial host isolated from deep-sea sediments

Mathias Middelboe, Sachia J Traving, Daniel Castillo, Panos G Kalatzis, Ronnie N Glud
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Abstract

Auxiliary metabolic genes encoded by bacteriophages can influence host metabolic function during infection. In temperate phages, auxiliary metabolic genes may increase host fitness when integrated as prophages into the host genome. However, little is known about the contribution of prophage-encoded auxiliary metabolic genes to host metabolic properties. In this study, we examined a temperate bacteriophage, and its piezotolerant Pseudomonas sp. host obtained from sediment samples collected from the Kermadec Trench at ~10 000 m water depth. Both the phage and host were present throughout the sediment profiles from the surface to 30 cm into the sediment, covering large gradients of environmental conditions. The host and phage each carried one chitinase gene, which differed from each other, suggesting that chitin degradation plays a role in their substrate supply. We demonstrated that prophage-encoded chitinase supported host chitin degradation and growth in the presence of chitin. Furthermore, prophage induction dynamics were strongly substrate-dependent, suggesting that the host controls the lysis-lysogeny switch in response to the presence of chitin, thus optimizing the trade-off between the loss of cells from prophage induction and prophage enhancement of host performance. Overall, the results demonstrate prophage-encoded auxiliary metabolic genes as collaborative goods for their hosts and emphasize the potential role of phage-host interactions in benthic biogeochemical cycling, as well as for the capability of deep-sea bacteria to efficiently adapt and thrive at a wide range of environmental conditions.
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原噬菌体编码的几丁质酶基因支持从深海沉积物中分离出来的细菌宿主的生长
噬菌体编码的辅助代谢基因可在感染过程中影响宿主的代谢功能。在温带噬菌体中,当辅助代谢基因作为噬菌体整合到宿主基因组中时,可能会提高宿主的适应能力。然而,人们对噬菌体编码的辅助代谢基因对宿主代谢特性的贡献知之甚少。在这项研究中,我们研究了一种温带噬菌体及其耐压假单胞菌宿主,宿主是从水深约 10,000 米的克马代克海沟采集的沉积物样本中获得的。噬菌体和宿主存在于从地表到 30 厘米深的整个沉积物剖面中,覆盖了较大的环境条件梯度。宿主和噬菌体各自携带一个几丁质酶基因,但基因之间存在差异,这表明几丁质降解在它们的底物供应中发挥了作用。我们证明,噬菌体编码的几丁质酶支持宿主几丁质的降解和在几丁质存在下的生长。此外,噬菌体的诱导动态强烈依赖于底物,这表明宿主会根据几丁质的存在控制裂解-溶解转换,从而在噬菌体诱导造成的细胞损失与噬菌体提高宿主性能之间实现最佳权衡。总之,研究结果表明噬菌体编码的辅助代谢基因是宿主的合作商品,强调了噬菌体-宿主相互作用在底栖生物地球化学循环中的潜在作用,以及深海细菌在各种环境条件下高效适应和繁衍的能力。
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