T4‐like myovirus community shaped by dispersal and deterministic processes in the South China Sea

Abstract

Summary As the most abundant and genetically diverse biological entities, viruses significantly influence ecological, biogeographical and evolutionary processes in the ocean. However, the biogeography of marine viruses and the drivers shaping viral community are unclear. Here, the biogeographic patterns of T4‐like viruses and the relative impacts of deterministic (environmental selection) and dispersal (spatial distance) processes were investigated in the northern South China Sea. The dominant viral operational taxonomic units were affiliated with previously defined Marine, Estuary, Lake and Paddy Groups. A clear viral biogeographic pattern was observed along the environmental gradient from the estuary to open sea. Marine Groups I and IV had a wide geographical distribution, whereas Marine Groups II, III and V were abundant in lower‐salinity continental or eutrophic environments. A significant distance‐decay pattern was noted for the T4‐like viral community, especially for those infecting cyanobacteria. Both deterministic and dispersal processes influenced viral community assembly, although environmental selection (e.g. temperature, salinity, bacterial abundance and community, etc.) had a greater impact than spatial distance. Network analysis confirmed the strong association between viral and bacterial community composition, and suggested a diverse ecological relationship (e.g. lysis, co‐infection or mutualistic) between and within viruses and their potential bacterial hosts.

Spatiotemporal Shift of T4-Like Phage Community Structure in the Three Largest Estuaries of China

“…The most abundant T4-like viruses of the Chinese estuarine ecosystems belonged to MG, which could be further subdivided into five MG subgroups (I to V) and two subgroups of Exo-T-even viruses that were predicted to infect cyanobacteria (Exo-T-evens–I and Exo-T-evens–II). Previous studies showed that MG I and MG IV had wide geographical distributions, whereas MG II, MG III, and MGV were abundant in low-salinity eutrophic environments ( 9 , 17 ). Sequences of the Exo-T-evens–I group were more closely related to the g23 genes of isolated cyanophages.…”

“…This indicated a large body of uncharacterized T4-like viruses in nature. All of the g23 OTUs obtained in Chinese estuaries, the representative g23 genes from different environments (e.g., marine, estuary, lake, paddy) ( 9 , 12 , 17 , 21 , 22 ), and the g23 genes of isolated T4-like phages in the NCBI NR database were used to build a phylogenetic tree. Overall, the phylogenetic profiles of the g23 genes formed three distinct clusters, which are referred to as Clusters I to III ( Fig.…”

“…Sequences of the Exo-T-evens–I group were more closely related to the g23 genes of isolated cyanophages. The Exo-T-evens–II group contained environmental-only sequences that were mainly derived from marine environments ( 9 , 17 , 20 ). MG sequences accounted for 59.8% to 92.0% (average, 76.5%) of the sequences in different samples, with the relative abundances of subgroups varying among samples ( Fig.…”

“…Phages within the T4-like subfamily typically share a core genome of 31 to 33 genes, among which g23 encodes the major capsid protein ( 10 , 11 , 15 ). To date, the diversity of the T4-like viruses has been investigated in various environments (e.g., seawater, lake, paddy water, rice field, wetland sediments); their prevalence across environments indicates that they play an important role in the diversity, community structure, evolution, and function of ecosystems ( 16 – 22 ). For example, infection by T4-like cyanophages inhibits CO 2 fixation in cyanobacteria ( 23 , 24 ); the T4-like viral lysis of the ubiquitous cyanobacteria and SAR11 releases cell contents to the organic carbon pool and accelerates carbon cycling in aquatic ecosystems ( 25 ).…”

“…For example, viral diversity has been investigated in the Jiulong River Estuary, revealing diverse and novel estuarine viral groups that adapted to local environments ( 18 , 31 ). However, numerous studies have suggested that viral communities temporally and spatially vary ( 17 , 32 , 33 ); and there have not been any spatiotemporal studies of viral communities in estuarine ecosystems. Therefore, in this study, we conducted a systematic investigation of the Chinese estuarine T4-like viral community at the three largest Chinese estuaries, which are located up to 2,000 km apart, in two different seasons (summer and winter) ( Fig.…”