Metagenome Mining Reveals Hidden Genomic Diversity of Pelagimyophages in Aquatic Environments

Abstract

The SAR11 clade is one of the most abundant bacterioplankton groups in surface waters of most of the oceans and lakes. However, only 15 SAR11 phages have been isolated thus far, and only one of them belongs to the Myoviridae family (pelagimyophages). Here, we have analyzed 26 sequences of myophages that putatively infect the SAR11 clade. They have been retrieved by mining ca. 45 Gbp aquatic assembled cellular metagenomes and viromes. Most of the myophages were obtained from the cellular fraction (0.2 μm), indicating a bias against this type of virus in viromes. We have found the first myophages that putatively infect Candidatus Fonsibacter (freshwater SAR11) and another group putatively infecting bathypelagic SAR11 phylogroup Ic. The genomes have similar sizes and maintain overall synteny in spite of low average nucleotide identity values, revealing high similarity to marine cyanomyophages. Pelagimyophages recruited metagenomic reads widely from several locations but always much more from cellular metagenomes than from viromes, opposite to what happens with pelagipodophages. Comparing the genomes resulted in the identification of a hypervariable island that is related to host recognition. Interestingly, some genes in these islands could be related to host cell wall synthesis and coinfection avoidance. A cluster of curli-related proteins was widespread among the genomes, although its function is unclear. IMPORTANCE SAR11 clade members are among the most abundant bacteria on Earth. Their study is complicated by their great diversity and difficulties in being grown and manipulated in the laboratory. On the other hand, and due to their extraordinary abundance, metagenomic data sets provide enormous richness of information about these microbes. Given the major role played by phages in the lifestyle and evolution of prokaryotic cells, the contribution of several new bacteriophage genomes preying on this clade opens windows into the infection strategies and life cycle of its viruses. Such strategies could provide models of attack of large-genome phages preying on streamlined aquatic microbes.

New viral biogeochemical roles revealed through metagenomic analysis of Lake Baikal

“…To our knowledge, no genomes of viruses infecting freshwater Methyloglobulus have been described. The gene content of these viruses included proteins involved in production of curly polymers and the ribosomal protein S21, which were previously detected in SAR11 phages [23] and a putative Polynucleobacter phage [5]. Interestingly, these viruses did not encode the diverse array of AMGs described for the methylotroph viruses from VP_139 and VP_266, possibly because these sequences do not represent the complete viral genome.…”

“…Among those assigned as viruses of bacteria (i.e., bacteriophages), the majority of sequences were predicted to infect Actinobacteriota (640), followed by Gammaproteobacteria (235), Bacteroidota (241) and Cyanobacteria (226), and Alphaproteobacteria (106). Although less frequent, some sequences were predicted to be derived from viruses that infect taxa with few or no isolated viruses such as Nitrospirota (9), Patescibacteria (14), and Crenarchaeota (23).…”

“…Consequently, little is known about the environmental drivers of community composition, biodiversity, and auxiliary metabolic genes in these ecosystems. The use of metagenomics has made it possible to describe viruses that infect the most representative freshwater microbes, such as acI Actinobacteria [20,21] and SAR11 [22,23]. Studies focused on Czech reservoirs and Lake Biwa (Japan) have reported on the extensive effects of stratification on freshwater viral communities, host prevalence, and on their key roles as recyclers of organic matter [21,24].…”

Culturing novel and abundant pelagiphages in the ocean

“…Other pelagiphage sequences reported in the literature were retrieved from culture‐independent single‐cell genomic or metagenomic studies (Mizuno et al ., 2013; Mizuno et al ., 2016; Martinez‐Hernandez et al ., 2017; Zaragoza‐Solas et al ., 2020). For example, a recent study reported 26 putative pelagimyophages that were retrieved from cellular metagenomes and viromes, revealing the genomic diversity of pelagimyophages (Zaragoza‐Solas et al ., 2020), and an uncultured single‐virus contig vSAG 37‐F6 has been identified as a pelagiphage (Martinez‐Hernandez et al ., 2017). To further explore the diversity of pelagiphages and establish more representative SAR11‐pelagiphage model systems for future investigations on pelagiphage genomic evolution and phage–host interactions, efforts are still needed to isolate and characterize more pelagiphages.…”

Tracking Double-Stranded DNA Bacteriophages and Their Hosts in a Deep Freshwater Lake by Integrating Metagenomics and The Hi-C Technique

“…However, the rapid development of viral metagenomics and bioinformatics has provided an opportunity to overcome these obstacles [5,6]. In recent years, large amounts of viral genomes, most of which are novel bacteriophages, have been identi ed from a variety of environments, such as marine environments [7,8], freshwater environments [9], hot spring mats [10], rhizosphere soils [11], and mangroves [12]. The ndings of these studies indicated that bacteriophages interacting with their hosts (bacteria and archaea), acted as key partners in multiple ecosystems.…”