Ecogenomics of Groundwater Phages Suggests Niche Differentiation Linked to Specific Environmental Tolerance

Kothari, Ankita; Roux, Simon; Zhang, Hanqiao; Prieto, Anatori; Soneja, Drishti; Chandonia, John-Marc; Spencer, Sarah J.; Wu, Xiaoqin; Altenburg, Sara; Deutschbauer, Adam M.; Arkin, Adam P.; Alm, Eric J.; Chakraborty, Romy; Mukhopadhyay, Aindrila

doi:10.1128/msystems.00537-21

Cited by 14 publications

(18 citation statements)

References 63 publications

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“…Since many viruses are strongly habitat-specific (Paez-Espino et al, 2016;Roux et al, 2012), the likelihood of sequencing novel viruses from an environment poorly represented in the databases is high. In addition to the lack of drinking water virome studies to date, the typical source waters (i.e., groundwater and surface water) for drinking water production have been less frequently studied than marine aquatic environments (Kallies et al, 2019;Kothari et al, 2021;Malki et al, 2020;Moon et al, 2020;Paez-Espino et al, 2016;Roux et al, 2012;Skvortsov et al, 2016). Of the 48,935 VPs (95% ANI across 85% of the contig) identified across all distribution systems, 156 viral populations were found in more than 10% of the samples.…”

Section: Viral Ecology Of Drinking Water Communitiesmentioning

confidence: 99%

A Snapshot of the Global Drinking Water Virome: Diversity and Metabolic Potential Vary with Residual Disinfectant Use

Hegarty

Dai

Raskin

et al. 2021

Preprint

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Viruses are important drivers of microbial community ecology and evolution, influencing microbial mortality, metabolism, and horizontal gene transfer. However, the effects of viruses remain largely unknown in many environments, including in drinking water systems. Drinking water metagenomic studies have offered a whole community perspective of bacterial impacts on water quality, but have not yet considered the influences of viruses. In this study, we address this gap by mining viral DNA sequences from publicly available drinking water metagenomes from distribution systems in six countries around the world. These datasets provide a snapshot of the taxonomic diversity and metabolic potential of the global drinking water virome, and provide an opportunity to investigate the effects of geography, climate, and drinking water treatment practices on viral diversity. Both environmental conditions and differences in sample processing were found to influence the viral composition. Using free chlorine as the residual disinfectant was associated with clear differences in viral taxonomic diversity and metabolic potential, with significantly fewer viral populations and less even viral community structures than observed in distribution systems without residual disinfectant. Additionally, significantly more viral-encoded genes involved in mitigating oxidative stress were observed in systems that use free chlorine, while significantly more viral genes involved in nitrogen metabolism were observed in systems that do not. Through this study, we have demonstrated that viral communities are diverse across drinking water systems and vary with the use of residual disinfectant. Our findings offer directions for future research to develop a more robust understanding of how virus-bacteria interactions in drinking water distribution systems affect water quality.

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Section: Viral Ecology Of Drinking Water Communitiesmentioning

confidence: 99%

A Snapshot of the Global Drinking Water Virome: Diversity and Metabolic Potential Vary with Residual Disinfectant Use

Hegarty

Dai

Raskin

et al. 2021

Preprint

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“…While most of the prophage sequences examined here do not encode antibiotic resistance genes or common virulence factors, many auxiliary metabolic genes were identified. Phage-encoded metabolic genes have been best studied in marine phages ( 83 , 84 ), and it was more recently explored in groundwater ( 85 ). Prior investigation of a few lytic P. aeruginosa -infecting phages found 3% of genes to be putative auxiliary metabolic genes, and phage-specific metabolic effects during infection have been observed ( 86 ).…”

Section: Discussionmentioning

confidence: 99%

Diversity of Pseudomonas aeruginosa Temperate Phages

Johnson

Banerjee

Putonti

2022

mSphere

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“…Elucidating the host range of phages is critical for understanding how they influence their microbial hosts, including their role in mobilizing DNA (12). CRISPR targeting data are frequently used to predict the bacterial hosts of phages (35)(36)(37)(38)(39); therefore, we took advantage of the extensive interspecies CRISPR targeting observed above (Fig. 7) to infer the hosts of known Neisseria prophages and predictions from all 3 tools.…”

Section: Many Known and Predicted Neisseria Prophages Have Additional...mentioning

confidence: 99%

“…Classifying phages is challenging due to their high genomic diversity, extensive mosaicism, and lack of universally shared genes (54)(55)(56)(57). Therefore, gene-sharing networks are commonly used to compare novel phages to previously identified phages (35,36,(57)(58)(59)(60)(61). Here, we used vConTACT v.2.0 (60,62) to assess whether the prophages we predicted are similar to known Neisseria phages (Table S1B) or phages that infect other bacterial taxa (i.e., other reference viruses; see Methods for details).…”

Section: Comparing Predictions To Known Phages Using Gene-sharing Net...mentioning

confidence: 99%

“…Importantly, sequence identity between the spacer and the MGE is required for immunity, which means that CRISPR arrays contain a record of previous encounters with MGEs within the sequences of their spacers. Therefore, this historical record can be used to infer the bacterial hosts of viruses (35)(36)(37)(38)(39). Approximately 40% of N. meningitidis genomes encode Type II-C CRISPR arrays (40,41), and multiple putative CRISPR systems have been identified in several commensal species (41)(42)(43).…”

Section: Introductionmentioning

confidence: 99%

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Prediction of prophages and their host ranges in pathogenic and commensal Neisseria species

Orazi

Collins

Whitaker

2021

Preprint

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The genus Neisseria includes two pathogenic species, N. gonorrhoeae and N. meningitidis, and numerous commensal species. Neisseria species frequently exchange DNA with one other, primarily via transformation and homologous recombination, and via multiple types of mobile genetic elements (MGEs). Few Neisseria bacteriophages (phages) have been identified and their impact on bacterial physiology is poorly understood. Furthermore, little is known about the range of species that Neisseria phages can infect. In this study, we used three virus prediction tools to scan 248 genomes of 21 different Neisseria species and identified 1302 unique predicted prophages. Using comparative genomics, we found that many predictions are dissimilar from other prophages and MGEs previously described to infect Neisseria species. We also identified similar predicted prophages in genomes of different Neisseria species. Additionally, we examined CRISPR-Cas targeting of each Neisseria genome and predicted prophage. While CRISPR targeting of chromosomal DNA appears to be common among several Neisseria species, we found that 20% of the prophages we predicted are targeted significantly more than the rest of the bacterial genome in which they were identified (i.e., backbone). Furthermore, many predicted prophages are targeted by CRISPR spacers encoded by other species. We then used these results to infer additional host species of known Neisseria prophages and predictions that are highly targeted relative to the backbone. Together, our results suggest that we have identified novel Neisseria prophages, several of which may infect multiple Neisseria species. These findings have important implications for understanding horizontal gene transfer between members of this genus.IMPORTANCEDrug-resistant N. gonorrhoeae is a major threat to human health. Commensal Neisseria species are thought to serve as reservoirs of antibiotic resistance and virulence genes for the pathogenic species N. gonorrhoeae and N. meningitidis. Therefore, it is important to understand both the diversity of mobile genetic elements (MGEs) that can mediate horizontal gene transfer within this genus, and the breadth of species these MGEs can infect. In particular, few bacteriophages (phages) have been identified and characterized in Neisseria species. In this study, we identified a large number of candidate phages integrated within the genomes of commensal and pathogenic Neisseria species, many of which appear to be novel phages. Importantly, we discovered extensive interspecies targeting of predicted phages by Neisseria CRISPR-Cas systems, which may reflect their movement between different species. Uncovering the diversity and host range of phages is essential for understanding how they influence the evolution of their microbial hosts.

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Ecogenomics of Groundwater Phages Suggests Niche Differentiation Linked to Specific Environmental Tolerance

Cited by 14 publications

References 63 publications

A Snapshot of the Global Drinking Water Virome: Diversity and Metabolic Potential Vary with Residual Disinfectant Use

A Snapshot of the Global Drinking Water Virome: Diversity and Metabolic Potential Vary with Residual Disinfectant Use

Diversity of Pseudomonas aeruginosa Temperate Phages

Prediction of prophages and their host ranges in pathogenic and commensal Neisseria species

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