Genome characteristics and environmental distribution of the first phage that infects the LD28 clade, a freshwater methylotrophic bacterial group

Abstract

Bacteriophages infecting major groups of freshwater heterotrophic bacteria have been rarely isolated, hampering analyses of freshwater viromes. Here, we report the isolation and genomic characterization of P19250A, the first phage that infects the LD28 clade, an abundant freshwater methylotrophic bacterial group. P19250A was isolated from Lake Soyang, an oligotrophic reservoir, using an LD28 strain as a host. Morphological and genomic analyses revealed that P19250A is a lytic siphovirus with a ∼38.6-kb genome. To analyze the distribution of P19250A genome within its habitat, six seasonal viral metagenome (virome) samples were prepared from Lake Soyang. Through binning analysis of freshwater viromes, P19250A was shown to be the most highly assigned freshwater phage that infects heterotrophic bacteria (up to 8.21%) in five viromes. Furthermore, when freshwater virome data collected worldwide were analyzed, P19250A genome also showed high abundance, especially in Lough Neagh, UK, where P19250A genome was recorded as the most abundant bacteriophage. From metagenome analysis, the proportion of P19250A-assigned reads showed seasonal fluctuation following the abundance of the LD28 clade in Lake Soyang. These results showed that P19250A would be an essential resource for analyses of freshwater viromes, and also suggest that phages of other abundant freshwater bacteria need to be isolated for better understanding of freshwater viruses.

Genome‐resolved viral and cellular metagenomes revealed potential key virus‐host interactions in a deep freshwater lake

“…The RVG was prepared by extracting 2621 genomes of isolated dsDNA prokaryotic viruses from the Virus‐Host Database (as of 6 February 2018) (Mihara et al ., ). The EVG was built based on 1811 genomes compiled for the previous study (Nishimura et al ., ) and augmented with the following datasets: (i) 125 842 mVCs (metagenomic Viral Contigs), which were generated from metagenomes deposited in the IMG/M database (Paez‐Espino et al ., ); (ii) 28 complete viral genomes retrieved from a Mediterranean deep‐ocean virome (Mizuno et al ., ); (iii) contigs assembled from six viromes collected seasonally from Lake Soyang (PRJEB15535) (Moon et al ., ); (iv) 488 contigs previously compiled from published freshwater viromes (Arkhipova et al ., ); and (v) 313 complete viral genomes recovered from Lake Neagh (Arkhipova et al ., ). In addition, the genomes of recently reported freshwater viruses, including the Synechococcus virus S‐EIV1 (Chénard et al ., ), eight actinoviruses (Ghai et al ., ), a LD28 virus (Moon et al ., ), two Comamonadaceae viruses (Moon et al ., ) and a Polynucleobacter virus (Cabello‐Yeves et al ., ) were compiled.…”

“…Through both cultivationdependent and -independent manners, viruses that infect major freshwater bacterioplankton lineages have been documented in the last few years, including those of Actinobacteria (Ghai et al, 2017), Polynucleobacter (Cabello-Yeves et al, 2017), LD28 (Ca. Methylopumilus) (Moon et al, 2017) and Comamonadaceae (Moon et al, 2018). Elucidating such predominant virus-host interactions is key to characterizing viruses playing central roles in the microbial ecosystem and biogeochemical cycling.…”

“…Elucidating such predominant virus-host interactions is key to characterizing viruses playing central roles in the microbial ecosystem and biogeochemical cycling. However, despite a growing number of viromic studies in freshwater systems (Skvortsov et al, 2016;Moon et al, 2017;Silva et al, 2017;Arkhipova et al, 2018), viruses infecting other typical freshwater bacterioplankton lineages, such as LD12 (Ca. Fonsibacter) (Henson et al, 2018) and Limnohabitans (Kasalický et al, 2013) have yet to be characterized.…”

Wide distribution of phage that infect freshwater SAR11 bacteria

“…In general, phage that infect major heterotrophic groups in freshwater ecosystems are largely unknown, with only a few cases reported recently, including phage of LD28 clade (' Ca . Methylopumilus planktonicus') (Moon et al 2017) and the Actinobacteria acl clade (Ghai et al 2017) . Phage that infect freshwater heterotrophic bacteria groups could shape the freshwater microbial assemblages and redistribute bacterially-derived compounds via the lysis of host cells.…”

Genomic and ecological study of two distinctive freshwater bacteriophages infecting a Comamonadaceae bacterium

“…However, contrast to the marine environment, only a few studies have been performed in lakes, which include researches on freshwater cyanophages 13 – 16 . Only recently, the phages infecting the LD28 bacterial clade were cultured from an oligotrophic freshwater lake 17 , and metagenome-assembled genomes of the phages that are considered to infect the acI clade were retrieved from viromes 18 . Each lake across the globe is confined and independent from one another such that each has its own unique ecological values, regardless of their geographic locations and variation in climates and environments.…”