Role of Filamentous Phage SW1 in Regulating the Lateral Flagella of Shewanella piezotolerans Strain WP3 at Low Temperatures

Abstract

b Low-temperature ecosystems represent the largest biosphere on Earth, and yet our understanding of the roles of bacteriophages in these systems is limited. Here, the influence of the cold-active filamentous phage SW1 on the phenotype and gene transcription of its host, Shewanella piezotolerans WP3 (WP3), was investigated by construction of a phage-free strain (WP3⌬SW1), which was compared with the wild-type strain. The expression of 49 genes, including 16 lateral flagellar genes, was found to be significantly influenced by SW1 at 4°C, as demonstrated by comparative whole-genome microarray analysis. WP3⌬SW1 was shown to have a higher production of lateral flagella than WP3 and enhanced swarming motility when cultivated on solid agar plates. Besides, SW1 has a remarkable impact on the expression of a variety of host genes in liquid culture, particularly the genes related to the membrane and to the production of lateral flagella. These results suggest that the deep-sea bacterium WP3 might balance the high-energy demands of phage maintenance and swarming motility at low temperatures. The phage SW1 is shown to have a significant influence on the swarming ability of the host and thus may play an important role in adjusting the fitness of the cells in the deep-sea environment. Due to a growing awareness that viruses, especially phages, are the most abundant biological entities on the planet and that they play an irreplaceable role in all types of ecosystems, research into phage-host interactions has garnered much attention. Cold environments, including glaciers, permafrost, and deep seas, cover a large part of the earth, and viruses are abundant and functional in these environments (1-4). Nevertheless, our understanding of phage-host interactions and of the extent to which phages influence the adaptation and evolution of hosts in lowtemperature environments is still incomplete (4).It is well known that the production and life cycles of temperate phages are under the strict control of the host (5-8). In recent years, it has become increasingly apparent that temperate phages could modulate the functions of host cells. In Escherichia coli, phages have been found to influence divergent functions of the lysogenic cell, including replication, transcription, translation, degradation, and proteolysis (9-13). Bacterial viruses can regulate the expression of host genes and decrease the growth rate of E. coli in energy-poor environments, thus increasing the population fitness of E. coli (14). Although they can be cryptic and lose their basic function during evolution, prophages allow bacteria to cope with adverse environments and osmotic, oxidative, and acid stresses, increasing host growth and biofilm formation (15, 16).The filamentous phages are temperate phages whose DNA integrates into the bacterial genome, and they become prophages and replicate with the host (17). In addition, some of the phage DNA can exist in the cytoplasm, such as in a plasmid, and this is called replicative-form (RF) DNA. The release of filamentous vir...

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

“…From this respect, the activity of deep‐sea sediment phage SW1 and its influence on bacterial host are worth to be investigated although some marine or terrestrial isolated phages have been studied. Our previous study has shown that the bathypelagic filamentous phage SW1 have a significant influence on transcription of 49 genes (including 16 lateral flagellar genes) and swarming motility of WP3 at 4°C (Jian et al ., ). In this study, the activity of SW1 was shown to significantly affect the growth and transcriptome of its deep‐sea bacterial host.…”

Isolation and Characterization of a Shewanella Phage–Host System from the Gut of the Tunicate, Ciona intestinalis

“…To date, a number of Shewanella phages (both lytic and temperate) have been described from marine and freshwater environments [17,18,19,20,21], and in Shewanella oneidensis , prophages have also been implicated as vital for biofilm formation through excision-mediated lysis [21]. Stably integrated prophage-like elements are common within the genomes of most marine bacterial species [22], and prophages are also thought to be important among bacteria that colonize the gut mucosa of animals [23], often forming biofilms [24,25].…”

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.…”