Deep sea sediments associated with cold seeps are a subsurface reservoir of viral diversity

Li, Zexin; Pan, Donald; Wei, Guangshan; Pi, Wei-Ling; Wang, Jiang-Hai; Peng, Yongyi; Zhang, Lu; Wang, Yong; Hubert, Casey R.J.; Dong, Xiyang

doi:10.1101/2020.09.08.284018

Cited by 17 publications

(41 citation statements)

References 78 publications

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“…S8). Notably, these results were signi cantly different from those obtained in a previous virome study in which most bacteriophages had greater abundance than their hosts [10,67]. The uncertainty provides another opportunity to use the Hi-C-based method to detect the bacteriophage-host relationship within prokaryotic cells instead of counting bacteriophages at lysis time.…”

Section: Bacteriophage-host Interactive Abundance Analysiscontrasting

confidence: 74%

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

Tao¹,

Gao²,

Li³

et al. 2020

Preprint

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Background: In aquatic ecosystems, bacteriophages play key roles in species diversity, host population dynamics and functional gene transfer. Due to a lack of high-throughput experimental tools to obtain robust associations between bacteriophages and hosts, the current metagenome-based phage community research generally predicts interactions based on various computational pipelines. In this study, by introducing an in vivo proximity-ligation chromosomal confirmation capture (Hi-C) technique combined with existing sequencing data from a freshwater metagenome study, we investigated double-stranded DNA (dsDNA) bacteriophages distribution, bacteriophage-host associations and abundance profiles at various depths in a deep alpine lake.Results: A total of 985 nonredundant viral genomes (containing 1,464 viral contigs measuring at least 10 kb) were identified using rigorous bioinformatic pipelines, and 67.3% of bacteriophages had never been reported previously. The bacteriophages had a significant depth-dependent distribution, and 56.9% of phage populations were only present in the epilimnion. Overall, 567 auxiliary metabolic genes (AMGs) were identified in 239 phages (24.26% of the total population). Hi-C reconstructed 58 bacteriophage-host association events encompassing eight bacterial phyla, among which 14 AMG-coding bacteriophages were clearly linked to their hosts. Three bacteriophages contained the mec gene, which was exactly complementary to their hosts in the sulfur-related pathway, and three other bacteriophages contained AMGs that likely participated in host fructose and mannose metabolism.Conclusions: The present study identifies bacteriophages in Lake Fuxian and describes the bacteriophages and their host dynamics along the depth profile. Our results indicate that metagenomics combined with the Hi-C technique has promise for future applications in high-throughput bacteriophage identification and bacteriophage-host association detection, which could further extend our knowledge of the functional roles played by bacteriophages in aquatic ecosystems.

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Section: Bacteriophage-host Interactive Abundance Analysiscontrasting

confidence: 74%

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

Tao¹,

Gao²,

Li³

et al. 2020

Preprint

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“…Aerobic methane-oxidizing bacteria (MOB), anaerobic methanotrophic (ANME) archaea, and sulfate-reducing bacteria (SRB) are three key groups of functional microorganisms in cold seeps sediments 1, 6, 9 . To identify them, we screened the 1261 MAGs for the presence of three functional genes: the particulate methane monooxygenase marker gene pmoA encoding for MOB, the methyl-coenzyme-M reductase marker gene mcrA for ANME archaea, and the dissimilatory sulfite reductase marker gene dsrA for SRB.…”

Section: Resultsmentioning

confidence: 99%

“…Cold seep microbiomes are reported to be locally selected and diversified (macrodiversity) by unique benthic biogeochemical conditions and environmental gradients such as for methane and sulfate concentrations 6, 7, 9, 39 . Evolutionary metrics (D’, SNVs/kbp, pN/pS) at the genome level showed significant differences ( P <0.001) among different cold seep sites (Supplementary Figure 13a) , indicating that different physicochemical conditions of various cold seep systems also influenced the intra-population diversity and evolutionary processes in microbial populations.…”

Section: Resultsmentioning

confidence: 99%

“…Based on amplicon sequencing of genetic markers and genome-resolved metagenomics, numerous studies have revealed the extensive macrodiversity (i.e. the measure of population diversity within a community 5 ) of archaeal and bacterial lineages and microbial metabolic versatility along different cold seep sites and sediment depths 1,[6][7][8][9] . Findings include the discovery of various lineages of archaeal anaerobic methanotrophs (ANME) and sulfate-reducing bacteria (SRB) as syntrophic aggregates to perform methane oxidation coupled to sulfate reduction at anoxic sediment layers 10,11 .…”

Section: Introductionmentioning

confidence: 99%

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Evolutionary ecology of microbial populations inhabiting deep sea sediments associated with cold seeps

Dong

Peng

Wang

et al. 2022

Preprint

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Deep sea cold seep sediments host abundant and diverse bacterial and archaeal populations that significantly influence biogeochemical cycles. While numerous studies have revealed the community structure and functional capabilities of cold seep microbiomes, little is known about their genetic heterogeneity within species. Here, we examined intraspecies diversity patterns of 39 abundant species identified in sediment layers down to 4.3 mbsf across six cold seep sites from around the world. These species were predicted to participate in methane oxidation and sulfate reduction, and based on their metabolic capabilities, grouped as aerobic methane-oxidizing bacteria (MOB), anaerobic methanotrophic archaea (ANME) and sulfate-reducing bacteria (SRB). These physiologically and phylogenetically diverse MOB, ANME and SRB display different degrees of intrapopulation sequence divergence and different evolutionary trajectories. Populations were in general characterized by low rates of homologous recombination and strong purifying selection with most of the nucleotide variation being synonymous. Functional genes related to methane (pmoAandmcrA) and sulfate (dsrA) metabolisms were found to be under strong purifying selection in the vast majority of species investigated, although examples of active positive selection were also observed. These genes differed in evolutionary trajectories across phylogenetic clades but are functionally conserved across cold seep sites. Intrapopulation diversification of MOB, ANME and SRB species as well as theirmcrAanddsrAgenes was observed to be depth-dependent and undergo divergent selection pressures throughout the sediment column. These results highlight the role of the interplay between ecological processes and the evolution of key bacteria and archaea in deep sea cold seep sediments and shed light on how microbial populations adapt in the subseafloor biosphere.

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“…To compare NBT sediment viruses ( n = 40,267) with other habitats, four ecological environmental virus data included: (1) GOV 2.0 seawater [ 28 ] ( n = 310,218); (2) wet-land sediment [ 29 ] ( n = 3344); (3) Stordalen thawing permafrost [ 30 ] ( n = 1907); (4) cold springs [ 31 ] ( n = 2885). For each viral contig, open reading frames (ORFs) were called using Prodigal v2.6.3 [ 21 ] and the predicted protein sequences were used as input for vConTACT2 [ 32 ].…”

Section: Methodsmentioning

confidence: 99%

Revealing the Viral Community in the Hadal Sediment of the New Britain Trench

Zhou

Chen

Zhang

et al. 2021

Genes

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Marine viruses are widely distributed and influence matter and energy transformation in ecosystems by modulating hosts’ metabolism. The hadal trenches represent the deepest marine habitat on Earth, for which the viral communities and related biogeochemical functions are least explored and poorly understood. Here, using the sediment samples (8720 m below sea level) collected from the New Britain Trench (NBT), we investigated the viral community, diversity, and genetic potentials in the hadal sediment habitat for the first time by deep shotgun metagenomic sequencing. We found the NBT sediment viral community was dominated by Siphoviridae, Myoviridae, Podoviridae, Mimiviridae, and Phycodnaviridae, which belong to the dsDNA viruses. However, the large majority of them remained uncharacterized. We found the hadal sediment virome had some common components by comparing the hadal sediment viruses with those of hadal aquatic habitats and those of bathypelagic and terrestrial habitats. It was also distinctive in community structure and had many novel viral clusters not associated with the other habitual virome included in our analyses. Further phylogenetic analysis on its Caudovirales showed novel diversities, including new clades specially evolved in the hadal sediment habitat. Annotation of the NBT sediment viruses indicated the viruses might influence microbial hydrocarbon biodegradation and carbon and sulfur cycling via metabolic augmentation through auxiliary metabolic genes (AMGs). Our study filled in the knowledge gaps on the virome of the hadal sediment habitats and provided insight into the evolution and the potential metabolic functions of the hadal sediment virome.

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Deep sea sediments associated with cold seeps are a subsurface reservoir of viral diversity

Cited by 17 publications

References 78 publications

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

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

Evolutionary ecology of microbial populations inhabiting deep sea sediments associated with cold seeps

Revealing the Viral Community in the Hadal Sediment of the New Britain Trench

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