Genomic analysis of Synechococcus phage S-B43 and its adaption to the coastal environment

Highlights

• AMGs carried by cyanophages isolated in different environments are not the same.

• Carrying of AMG in cyanophage is related to host and environment.

• The AMGs carried by the cyanophages help them and their host adapt to the environment.

Abstract

Synechococcus dominate picocyanobacterial communities in coastal environments. However, only a few Synechococcus phages have been described from the coastal seas of the Northwest Pacific Ocean. Here a new Synechococcus phage, S-B43 was isolated from the Bohai Sea, a semi-closed coastal sea of the Northwest Pacific Ocean. S-B43 is a member of Myoviridae, containing 275 predicted open reading frames. Fourteen auxiliary metabolic genes (AMG) were identified from the genome of S-B43, including five photosynthetic associated genes and several AMGs related to its adaption to the high turbidity and eutrophic coastal environment with a low ratio of phosphorus to nitrogen (HNLP). The occurrences of 31 AMGs among 34 cyanophage genomes indicates that AMGs zwf, gnd, speD, petF and those coding for FECH and thioredoxin were more common in coastal areas than in the open ocean and AMGs pebS and ho1 were more prevalent in the open ocean. The occurrence of cyanophage AMGs in different environments might be a reflection of the environmental adaption of their hosts. This study contributes to our understanding of the interactions between cyanobacteria and cyanophages and their environmental adaption to the coastal environment.

Introduction

Picocyanobacteria of the Synechococcus and Prochlorococcus genera are the most abundant oxygenic phototrophs and contribute more than half of the primary production in oligotrophic oceans (Field et al., 1998; Mann et al., 2005; Sullivan et al., 2005; Flombaum et al., 2013). Synechococcus are distributed in the global oceans from pole to pole while Prochlorococcus are restricted to the tropical and subtropical oceans (Partensky et al., 1999; Zeidner et al., 2005;, Huang et al., 2015). Cyanophages, viruses that infect cyanobacteria, are widespread and abundant in coastal seas and the euphotic zone of the open ocean (Suttle, 2000).

To date, all cyanophages isolated belong to three families of the Caudovirales order– dsDNA viruses with tails: Myoviridae (contractile tails), Podoviridae (short tails) and Siphoviridae (long non-contractile tails) (Suttle, 2000; Chen and Lu, 2002; Sullivan et al., 2003; Enav et al., 2018). The length of these genomes is generally 40−230 kb and they usually contain many unknown gene components (Finke and Suttle, 2019). Cyanophages can influence the abundance and community structure of cyanobacteria through lytic or lysogenic infection (Thingstad, 2000; Sullivan et al., 2005; Zeidner et al., 2005). Further, cyanophages can also impact host evolution, horizontal gene transfer and their antagonistic coevolution with cyanobacteria (Buckling and Rainey, 2002).

Cyanophages commonly contain auxiliary metabolic genes (AMGs), which can influence the metabolism of their hosts through the expression of AMGs during infection (Lindell et al., 2004; Sullivan et al., 2005; Breitbart et al., 2007; Labrie et al., 2013). These AMGs are associated with a variety of functions including photosynthesis (Mann et al., 2003; Sharon et al., 2011; Philosof et al., 2011), carbon metabolism (Thompson et al., 2011), nucleic acid synthesis and metabolism (Dwivedi et al., 2013; Enav et al., 2014), and stress tolerance (Lindell et al., 2005; Kelly et al., 2013; Enav et al., 2014). AMGs related to photosynthesis, such as psbA (photosystem II D1 protein,), psbD (photosystem II D2 protein), and hli (highlight-inducible protein) are expressed during phage infection (Lindell et al., 2005; Clokie and Mann, 2006; Sieradzki et al., 2019) and thus may make more energy available for phage reproduction (Lindell et al., 2005; Clokie and Mann, 2006; Hellweger, 2009; Millard et al., 2009). An analysis of metagenomic samples has shown that AMGs are abundant, diverse, and widespread in the oceans (Williamson et al., 2008). Recent studies on cyanophage isolates suggest that the gain and loss of AMGs represents an adaptation to selection pressures (Crummett et al., 2016), such as phosphate stress (Kelly et al., 2013). However, our knowledge of the relationship between cyanophage AMGs and environment preference is limited, especially in the eutrophic coastal seas of the Northwest Pacific Ocean.

Here, we report a new cyanophage isolated from the Bohai Sea, a semi-closed and eutrophic coastal sea of the Northwest Pacific Ocean. The environment of this sea is characterized by high turbidity and eutrophication. However, because of the low phosphorus - nitrogen ratio (high N low P, HNLP), there is a potential for phosphorous limiting eutrophication. (Liu et al., 2013; Zhang et al., 2019). The biological characteristics, whole genome of Synechococcus phage S-B43 and the occurrence of AMGs in the genomes of 34 cyanophages were analyzed. The genome of Synechococcus phage S-B43 contained AMGs and functional genes that could contribute to its adaption to the environment.