A Novel and Ubiquitous Marine Methylophage Provides Insights into Viral-Host Coevolution and Possible Host-Range Expansion in Streamlined Marine Heterotrophic Bacteria

Buchholz, Holger H; Bolaños, Luis M.; Bell, Ashley; Michelsen, Michelle L.; Allen, Michael J.; Temperton, Ben

doi:10.1128/aem.00255-22

Cited by 5 publications

(5 citation statements)

References 130 publications

(204 reference statements)

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“…The G + C content of both phage genomes is approximately 34%, which is similar to that of their host FZCC0133 (33.1%). Their G + C content is slightly higher than that of the first OM43 phage Venkman (31.9%) ( 23 ) but lower than those of the previously reported OM43 phages MEP301 (44.4%) ( 38 ) and Melnitz (37.6%) ( 39 ). MEP401 and MEP402 encode 67 and 69 open reading frames (ORFs), respectively.…”

Section: Resultscontrasting

confidence: 62%

“…To date, only three OM43 phage isolates have been reported, phage Venkman (EXVC282S), isolated from the western English Channel on OM43 strain H5P1 ( 23 ), phage MEP301, isolated from the Bohai Sea on OM43 strain HTCC2181 ( 38 ), and phage Melnitz (EXVC044M), isolated from the western English Channel and Sargasso Sea on OM43 strain H5P1 ( 39 ). These three OM43 phages were classified into three distinct viral groups.…”

Section: Introductionmentioning

confidence: 99%

“…Venkman and MEP301 both have an icosahedral head and a short tail, belonging to two distinct viral groups ( 23 , 38 ). Melnitz has a myovirus morphotype and is most closely related to pelagiphage Mosig and HTVC008M ( 39 ). Metagenomic analysis showed that most OM43 phages were correlated with temperature, having a higher relative abundance in cold waters ( 38 , 39 ).…”

Section: Introductionmentioning

confidence: 99%

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Genomic diversity and biogeographic distributions of a novel lineage of bacteriophages that infect marine OM43 bacteria

Yang,

Du,

Zhang

et al. 2023

Microbiol Spectr

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The marine methylotrophic OM43 clade is considered an important bacterial group in coastal microbial communities. OM43 bacteria, which are closely related to phytoplankton blooms, have small cell sizes and streamlined genomes. Bacteriophages profoundly shape the evolutionary trajectories, population dynamics, and physiology of microbes. The prevalence and diversity of several phages that infect OM43 bacteria have been reported. In this study, we isolated and sequenced two novel OM43 phages, MEP401 and MEP402. These phages share 90% of their open reading frames (ORFs) and are distinct from other known phage isolates. Furthermore, a total of 99 metagenomic viral genomes (MVGs) closely related to MEP401 and MEP402 were identified. Phylogenomic analyses suggest that MEP401, MEP402, and these identified MVGs belong to a novel subfamily in the family Zobellviridae and that they can be separated into two groups. Group I MVGs show conserved whole-genome synteny with MEP401, while group II MVGs possess the MEP401-type DNA replication module and a distinct type of morphogenesis and packaging module, suggesting that genomic recombination occurred between phages. Most members in these two groups were predicted to infect OM43 bacteria. Metagenomic read-mapping analysis revealed that the phages in these two groups are globally ubiquitous and display distinct biogeographic distributions, with some phages being predominant in cold regions, some exclusively detected in estuarine stations, and others displaying wider distributions. This study expands our knowledge of the diversity and ecology of a novel phage lineage that infects OM43 bacteria by describing their genomic diversity and global distribution patterns. IMPORTANCE OM43 phages that infect marine OM43 bacteria are important for host mortality, community structure, and physiological functions. In this study, two OM43 phages were isolated and characterized. Metagenomic viral genome (MVG) retrieval using these two OM43 phages as baits led to the identification of two phage groups of a new subfamily in the family Zobellviridae . We found that group I MVGs share similar genomic content and arrangement with MEP401 and MEP402, whereas group II MVGs only possess the MEP401-type DNA replication module. Metagenomic mapping analysis suggests that members in these two groups are globally ubiquitous with distinct distribution patterns. This study provides important insights into the genomic diversity and biogeography of the OM43 phages in the global ocean.

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Section: Resultscontrasting

confidence: 62%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Genomic diversity and biogeographic distributions of a novel lineage of bacteriophages that infect marine OM43 bacteria

Yang,

Du,

Zhang

et al. 2023

Microbiol Spectr

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“…Other pelagiphage types had 15–33 shared core genes in their respective groups (Supplementary Table 2 ). No core genes were shared between Ubiqueviridae and phages of other morphotypes that have been experimentally confirmed to infect Pelagibacter [ 22 – 24 , 27 , 41 ], the unassigned siphophage Kolga, and myophages Melnitz and HTVC008M.…”

Section: Resultsmentioning

confidence: 99%

Novel pelagiphage isolate Polarivirus skadi is a polar specialist that dominates SAR11-associated bacteriophage communities at high latitudes

et al. 2023

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The SAR11 clade are the most abundant members of surface marine bacterioplankton and a critical component of global biogeochemical cycles. Similarly, pelagiphages that infect SAR11 are ubiquitous and highly abundant in the oceans. Pelagiphages are predicted to shape SAR11 community structures and increase carbon turnover throughout the oceans. Yet, ecological drivers of host and niche specificity of pelagiphage populations are poorly understood. Here we report the global distribution of a novel pelagiphage called “Polarivirus skadi”, which is the sole representative of a novel genus. P. skadi was isolated from the Western English Channel using a cold-water ecotype of SAR11 as bait. P. skadi is closely related to the globally dominant pelagiphage HTVC010P. Along with other HTVC010P-type viruses, P. skadi belongs to a distinct viral family within the order Caudovirales, for which we propose the name Ubiqueviridae. Metagenomic read recruitment identified P. skadi as one of the most abundant pelagiphages on Earth. P. skadi is a polar specialist, replacing HTVC010P at high latitudes. Experimental evaluation of P. skadi host range against cold- and warm-water SAR11 ecotypes supported cold-water specialism. Relative abundance of P. skadi in marine metagenomes correlated negatively with temperature, and positively with nutrients, available oxygen, and chlorophyll concentrations. In contrast, relative abundance of HTVC010P correlated negatively with oxygen and positively with salinity, with no significant correlation to temperature. The majority of other pelagiphages were scarce in most marine provinces, with a few representatives constrained to discrete ecological niches. Our results suggest that pelagiphage populations persist within a global viral seed bank, with environmental parameters and host availability selecting for a few ecotypes that dominate ocean viromes.

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“…More recently, observations of very low levels of Prochlorococcus infection (0.35-1.6%) in oligotrophic waters with high cyanophage abundance has been hypothesised to result from a combination of host resistance, low phage adsorption rates and rapid loss of infectivity of virions 18 . To date, our understanding of the structure of the viral communities in the Sargasso Sea have been limited to seasonal patterns in abundances of viral-like particles 11 and genomic analysis of isolated phages 14,[19][20][21][22] .…”

mentioning

confidence: 99%

Long-read powered viral metagenomics in the oligotrophic Sargasso Sea

Warwick-Dugdale,

Tian,

Michelsen

et al. 2024

Nat Commun

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Dominant microorganisms of the Sargasso Sea are key drivers of the global carbon cycle. However, associated viruses that shape microbial community structure and function are not well characterised. Here, we combined short and long read sequencing to survey Sargasso Sea phage communities in virus- and cellular fractions at viral maximum (80 m) and mesopelagic (200 m) depths. We identified 2,301 Sargasso Sea phage populations from 186 genera. Over half of the phage populations identified here lacked representation in global ocean viral metagenomes, whilst 177 of the 186 identified genera lacked representation in genomic databases of phage isolates. Viral fraction and cell-associated viral communities were decoupled, indicating viral turnover occurred across periods longer than the sampling period of three days. Inclusion of long-read data was critical for capturing the breadth of viral diversity. Phage isolates that infect the dominant bacterial taxa Prochlorococcus and Pelagibacter, usually regarded as cosmopolitan and abundant, were poorly represented.

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A Novel and Ubiquitous Marine Methylophage Provides Insights into Viral-Host Coevolution and Possible Host-Range Expansion in Streamlined Marine Heterotrophic Bacteria

Cited by 5 publications

References 130 publications

Genomic diversity and biogeographic distributions of a novel lineage of bacteriophages that infect marine OM43 bacteria

Genomic diversity and biogeographic distributions of a novel lineage of bacteriophages that infect marine OM43 bacteria

Novel pelagiphage isolate Polarivirus skadi is a polar specialist that dominates SAR11-associated bacteriophage communities at high latitudes

Long-read powered viral metagenomics in the oligotrophic Sargasso Sea

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