{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,30]],"date-time":"2026-07-30T09:02:55Z","timestamp":1785402175645,"version":"3.56.0"},"reference-count":98,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2026,4,25]],"date-time":"2026-04-25T00:00:00Z","timestamp":1777075200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Hainan Provincial Natural Science Foundation of China","award":["423RC548"],"award-info":[{"award-number":["423RC548"]}]},{"DOI":"10.13039\/501100008111","name":"Science and Technology Talent Innovation Project of Hainan Province","doi-asserted-by":"publisher","award":["KJRC2023C14"],"award-info":[{"award-number":["KJRC2023C14"]}],"id":[{"id":"10.13039\/501100008111","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["41506139"],"award-info":[{"award-number":["41506139"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"award":["41506139"],"award-info":[{"award-number":["41506139"]}],"id":[{"id":"https:\/\/ror.org\/01h0zpd94","id-type":"ROR","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>Viruses are key regulators of marine microbial communities, yet their temporal dynamics in tropical intertidal sediments remain poorly characterized. We conducted a year-long metagenomic survey of sandy intertidal sediments in Sanya Bay (60 monthly samples from five sites) to examine viral taxonomy, community structure, lytic proteins, and auxiliary metabolic genes (AMGs). Within the classifiable fraction, the assemblages were consistently dominated by Assiduviridae. However, NMDS analysis revealed a significant overall seasonal shift, with October\u2013December samples separating from the rest of the year. Co-occurrence network analysis identified five co-occurrence modules with distinct temporal patterns, alongside a concurrent decline in module abundance and lytic proteins in October. Functional annotation showed that cysteine and methionine metabolism, primarily driven by DNA methyltransferases, was identified as a highly represented AMG category among the annotated functions, while other pathways displayed seasonal variability. Collectively, these findings suggest that although characterized by a classifiable fraction dominated by Assiduviridae, the highly complex tropical intertidal viral communities undergo substantial seasonal reorganization in structure and functional potential.<\/jats:p>","DOI":"10.3390\/v18050500","type":"journal-article","created":{"date-parts":[[2026,4,29]],"date-time":"2026-04-29T07:43:51Z","timestamp":1777448631000},"page":"500","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Annual Dynamics and Functional Traits of Viral Communities in Tropical Intertidal Sands of Sanya Bay"],"prefix":"10.3390","volume":"18","author":[{"ORCID":"https:\/\/orcid.org\/0009-0004-9403-0450","authenticated-orcid":false,"given":"Zijia","family":"Wang","sequence":"first","affiliation":[{"name":"Institute of Deep-Sea Science and Engineering, Chinese Academy of Sciences, Sanya 572000, China"},{"name":"College of Marine Sciences, University of Chinese Academy of Sciences, Beijing 100049, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0008-5927-423X","authenticated-orcid":false,"given":"Zongminghan","family":"Liu","sequence":"additional","affiliation":[{"name":"Institute of Deep-Sea Science and Engineering, Chinese Academy of Sciences, Sanya 572000, China"},{"name":"College of Marine Sciences, University of Chinese Academy of Sciences, Beijing 100049, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Juntao","family":"Zeng","sequence":"additional","affiliation":[{"name":"Institute of Deep-Sea Science and Engineering, Chinese Academy of Sciences, Sanya 572000, China"},{"name":"College of Marine Sciences, University of Chinese Academy of Sciences, Beijing 100049, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiwei","family":"Li","sequence":"additional","affiliation":[{"name":"Institute of Deep-Sea Science and Engineering, Chinese Academy of Sciences, Sanya 572000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiahao","family":"Cheng","sequence":"additional","affiliation":[{"name":"Institute of Deep-Sea Science and Engineering, Chinese Academy of Sciences, Sanya 572000, China"},{"name":"College of Marine Sciences, University of Chinese Academy of Sciences, Beijing 100049, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaoxue","family":"Qi","sequence":"additional","affiliation":[{"name":"Institute of Deep-Sea Science and Engineering, Chinese Academy of Sciences, Sanya 572000, China"},{"name":"College of Marine Sciences, University of Chinese Academy of Sciences, Beijing 100049, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jingwen","family":"Li","sequence":"additional","affiliation":[{"name":"Institute of Deep-Sea Science and Engineering, Chinese Academy of Sciences, Sanya 572000, China"},{"name":"College of Marine Sciences, University of Chinese Academy of Sciences, Beijing 100049, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8844-2107","authenticated-orcid":false,"given":"Shijie","family":"Bai","sequence":"additional","affiliation":[{"name":"Institute of Deep-Sea Science and Engineering, Chinese Academy of Sciences, Sanya 572000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,4,25]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1146\/annurev-marine-120709-142805","article-title":"Marine Viruses: Truth or Dare","volume":"4","author":"Breitbart","year":"2012","journal-title":"Annu. Rev. Mar. Sci."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"4429","DOI":"10.1128\/AEM.00029-07","article-title":"Viral Abundance, Decay, and Diversity in the Meso- and Bathypelagic Waters of the North Atlantic","volume":"73","author":"Parada","year":"2007","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"e00052-20","DOI":"10.1128\/JB.00052-20","article-title":"Are There 1031 Virus Particles on Earth, or More, or Fewer?","volume":"202","author":"Mushegian","year":"2020","journal-title":"J. Bacteriol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"7806","DOI":"10.1038\/s41467-025-63162-2","article-title":"Metagenomic analysis reveals how multiple stressors disrupt virus\u2013host interactions in multi-trophic freshwater mesocosms","volume":"16","author":"Wang","year":"2025","journal-title":"Nat. Commun."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"754","DOI":"10.1038\/s41564-018-0166-y","article-title":"Phage puppet masters of the marine microbial realm","volume":"3","author":"Breitbart","year":"2018","journal-title":"Nat. Microbiol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1486","DOI":"10.1007\/s11427-018-9414-7","article-title":"Diversity, evolutionary contribution and ecological roles of aquatic viruses","volume":"61","author":"Zhang","year":"2018","journal-title":"Sci. China Life Sci."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1007\/BF00166813","article-title":"The significance of viruses to mortality in aquatic microbial communities","volume":"28","author":"Suttle","year":"1994","journal-title":"Microb. Ecol."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Abdulrahman Ashy, R., Suttle, C.A., and Agust\u00ed, S. (2021). Moderate Seasonal Dynamics Indicate an Important Role for Lysogeny in the Red Sea. Microorganisms, 9.","DOI":"10.3390\/microorganisms9061269"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"801","DOI":"10.1038\/nrmicro1750","article-title":"Marine viruses\u2014Major players in the global ecosystem","volume":"5","author":"Suttle","year":"2007","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"e1602565","DOI":"10.1126\/sciadv.1602565","article-title":"Unveiling the role and life strategies of viruses from the surface to the dark ocean","volume":"3","author":"Lara","year":"2017","journal-title":"Sci. Adv."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"187","DOI":"10.3354\/ame027187","article-title":"Regeneration of dissolved organic matter by viral lysis in marine microbial communities","volume":"27","author":"Middelboe","year":"2002","journal-title":"Aquat. Microb. Ecol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1991","DOI":"10.1128\/aem.62.6.1991-1997.1996","article-title":"Effects of viruses on nutrient turnover and growth efficiency of noninfected marine bacterioplankton","volume":"62","author":"Middelboe","year":"1996","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1451","DOI":"10.1016\/j.cell.2019.11.018","article-title":"The Biomass Composition of the Oceans: A Blueprint of Our Blue Planet","volume":"179","author":"Milo","year":"2019","journal-title":"Cell"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1552","DOI":"10.1038\/s41396-023-01431-y","article-title":"Metagenome-derived virus-microbe ratios across ecosystems","volume":"17","author":"Krupovic","year":"2023","journal-title":"ISME J."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1046\/j.1462-2920.2003.00539.x","article-title":"Are viruses driving microbial diversification and diversity?","volume":"6","author":"Weinbauer","year":"2004","journal-title":"Environ. Microbiol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1038\/nrmicro3404","article-title":"Rising to the challenge: Accelerated pace of discovery transforms marine virology","volume":"13","author":"Brum","year":"2015","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"222","DOI":"10.1038\/s41586-018-0805-8","article-title":"The global distribution and trajectory of tidal flats","volume":"565","author":"Murray","year":"2019","journal-title":"Nature"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1038\/s41522-024-00522-8","article-title":"Temporal turnover of viral biodiversity and functional potential in intertidal wetlands","volume":"10","author":"Ji","year":"2024","journal-title":"npj Biofilms Microbiomes"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1146\/annurev-marine-051413-012706","article-title":"Benthic Exchange and Biogeochemical Cycling in Permeable Sediments","volume":"6","author":"Huettel","year":"2014","journal-title":"Annu. Rev. Mar. Sci."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Vandieken, V., Sabelhaus, L., and Engelhardt, T. (2017). Virus Dynamics Are Influenced by Season, Tides and Advective Transport in Intertidal, Permeable Sediments. Front. Microbiol., 8.","DOI":"10.3389\/fmicb.2017.02526"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.zool.2018.02.004","article-title":"Metaorganisms in extreme environments: Do microbes play a role in organismal adaptation?","volume":"127","author":"Bang","year":"2018","journal-title":"Zoology"},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Yi, J., Lo, L.S.H., and Cheng, J. (2020). Dynamics of Microbial Community Structure and Ecological Functions in Estuarine Intertidal Sediments. Front. Mar. Sci., 7.","DOI":"10.3389\/fmars.2020.585970"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"466","DOI":"10.1038\/nature17193","article-title":"Lytic to temperate switching of viral communities","volume":"531","author":"Knowles","year":"2016","journal-title":"Nature"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1038\/s41579-021-00602-y","article-title":"Interactions between bacterial and phage communities in natural environments","volume":"20","author":"Chevallereau","year":"2022","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Wei, M., and Xu, K. (2020). New Insights Into the Virus-to-Prokaryote Ratio (VPR) in Marine Sediments. Front. Microbiol., 11.","DOI":"10.3389\/fmicb.2020.01102"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"132087","DOI":"10.1016\/j.jhazmat.2023.132087","article-title":"Unraveling antibiotic resistomes associated with bacterial and viral communities in intertidal mudflat aquaculture area","volume":"459","author":"Zhu","year":"2023","journal-title":"J. Hazard. Mater."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1016\/j.seares.2013.11.011","article-title":"Microbial interactions in marine water amended by eroded benthic biofilm: A case study from an intertidal mudflat","volume":"92","author":"Ory","year":"2014","journal-title":"J. Sea Res."},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Montani\u00e9, H., De Crignis, M.G., and Lavaud, J. (2015). Viral Impact on Prokaryotic and Microalgal Activities in the Microphytobenthic Biofilm of an Intertidal Mudflat (French Atlantic Coast). Front. Microbiol., 6.","DOI":"10.3389\/fmicb.2015.01214"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1186\/s40064-015-0977-8","article-title":"Microscale spatial distributions of microbes and viruses in intertidal photosynthetic microbial mats","volume":"4","author":"Carreira","year":"2015","journal-title":"SpringerPlus"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"180","DOI":"10.1016\/S0025-326X(03)00070-5","article-title":"The status of the ecological environment and a proposed protection strategy in Sanya Bay, Hainan Island, China","volume":"47","author":"Huang","year":"2003","journal-title":"Mar. Pollut. Bull."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"783","DOI":"10.3989\/scimar.2010.74n4783","article-title":"Phytoplankton distribution and their relationship to environmental variables in Sanya Bay, South China Sea","volume":"74","author":"Zhang","year":"2010","journal-title":"Sci. Mar."},{"key":"ref_32","first-page":"168","article-title":"Spatial and temporal variability of copepod assemblages in Sanya Bay, northern South China Sea","volume":"7","author":"Li","year":"2016","journal-title":"Reg. Stud. Mar. Sci."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1007\/s13131-020-1583-3","article-title":"Dietary separation between co-occurring copepods in a food-limited tropical coral reef of the Sanya Bay","volume":"39","author":"Hu","year":"2020","journal-title":"Acta Oceanol. Sin."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"57","DOI":"10.2478\/s13545-012-0007-1","article-title":"Monsoon-driven dynamics of environmental factors and phytoplankton in tropical Sanya Bay, South China sea","volume":"41","author":"Wu","year":"2012","journal-title":"Oceanol. Hydrobiol. Stud."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"76784","DOI":"10.1007\/s11356-023-27527-8","article-title":"Spatiotemporal variations and impact factors of nutrients in the Sanya Bay, northern South China Sea","volume":"30","author":"Geng","year":"2023","journal-title":"Environ. Sci. Pollut. Res."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"884","DOI":"10.1093\/bioinformatics\/bty560","article-title":"fastp: An ultra-fast all-in-one FASTQ preprocessor","volume":"34","author":"Chen","year":"2018","journal-title":"Bioinformatics"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"824","DOI":"10.1101\/gr.213959.116","article-title":"metaSPAdes: A new versatile metagenomic assembler","volume":"27","author":"Nurk","year":"2017","journal-title":"Genome Res"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"e118","DOI":"10.1002\/imt2.118","article-title":"ViWrap: A modular pipeline to identify, bin, classify, and predict viral-host relationships for viruses from metagenomes","volume":"2","author":"Zhou","year":"2023","journal-title":"iMeta"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1186\/s40168-020-00867-0","article-title":"VIBRANT: Automated recovery, annotation and curation of microbial viruses, and evaluation of viral community function from genomic sequences","volume":"8","author":"Kieft","year":"2020","journal-title":"Microbiome"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1186\/s40168-020-00990-y","article-title":"VirSorter2: A multi-classifier, expert-guided approach to detect diverse DNA and RNA viruses","volume":"9","author":"Guo","year":"2021","journal-title":"Microbiome"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"e83","DOI":"10.1093\/nar\/gkac341","article-title":"vRhyme enables binning of viral genomes from metagenomes","volume":"50","author":"Kieft","year":"2022","journal-title":"Nucleic Acids Res."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"2864","DOI":"10.1038\/ismej.2017.126","article-title":"dRep: A tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication","volume":"11","author":"Olm","year":"2017","journal-title":"ISME J."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"i25","DOI":"10.1093\/bioinformatics\/btab293","article-title":"Bacteriophage classification for assembled contigs using graph convolutional network","volume":"37","author":"Shang","year":"2021","journal-title":"Bioinformatics"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"btaf147","DOI":"10.1093\/bioinformatics\/btaf147","article-title":"CoverM: Read alignment statistics for metagenomics","volume":"41","author":"Aroney","year":"2025","journal-title":"Bioinformatics"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"3094","DOI":"10.1093\/bioinformatics\/bty191","article-title":"Minimap2: Pairwise alignment for nucleotide sequences","volume":"34","author":"Li","year":"2018","journal-title":"Bioinformatics"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"8883","DOI":"10.1093\/nar\/gkaa621","article-title":"DRAM for distilling microbial metabolism to automate the curation of microbiome function","volume":"48","author":"Shaffer","year":"2020","journal-title":"Nucleic Acids Res."},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Eddy, S.R. (2011). Accelerated Profile HMM Searches. PLoS Comput. Biol., 7.","DOI":"10.1371\/journal.pcbi.1002195"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"wraf200","DOI":"10.1093\/ismejo\/wraf200","article-title":"Diversity and evolution of prokaryotic viral lytic proteins","volume":"19","author":"Yang","year":"2025","journal-title":"ISME J."},{"key":"ref_49","unstructured":"R Core Team (2025). R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"e32","DOI":"10.1002\/imt2.32","article-title":"ggClusterNet: An R package for microbiome network analysis and modularity-based multiple network layouts","volume":"1","author":"Wen","year":"2022","journal-title":"iMeta"},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Deng, Y., Jiang, Y.-H., Yang, Y., He, Z., Luo, F., and Zhou, J. (2012). Molecular ecological network analyses. BMC Bioinform., 13.","DOI":"10.1186\/1471-2105-13-113"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"D776","DOI":"10.1093\/nar\/gkaf1159","article-title":"Virus taxonomy: The database of the International Committee on Taxonomy of Viruses","volume":"54","author":"Black","year":"2026","journal-title":"Nucleic Acids Res."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1007\/s00705-022-05694-2","article-title":"Abolishment of morphology-based taxa and change to binomial species names: 2022 taxonomy update of the ICTV bacterial viruses subcommittee","volume":"168","author":"Turner","year":"2023","journal-title":"Arch. Virol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"555","DOI":"10.1038\/s41396-021-01097-4","article-title":"Highly diverse flavobacterial phages isolated from North Sea spring blooms","volume":"16","author":"Bartlau","year":"2022","journal-title":"ISME J."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"3228","DOI":"10.1038\/s41467-024-47600-1","article-title":"Diversity and potential host-interactions of viruses inhabiting deep-sea seamount sediments","volume":"15","author":"Yu","year":"2024","journal-title":"Nat. Commun."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"12798","DOI":"10.1073\/pnas.1305956110","article-title":"Twelve previously unknown phage genera are ubiquitous in global oceans","volume":"110","author":"Holmfeldt","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_57","first-page":"34","article-title":"Distribution characteristics of primary production and its influence factors in Sanya Bay, Hainan Island during Northeast Monsoon Period","volume":"28","author":"Song","year":"2009","journal-title":"Mar. Sci. Bull."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"121620","DOI":"10.1016\/j.watres.2024.121620","article-title":"Phage phylogeny, molecular signaling, and auxiliary antimicrobial resistance in aerobic and anaerobic membrane bioreactors","volume":"256","author":"Wang","year":"2024","journal-title":"Water Res."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"8611","DOI":"10.1038\/s41467-024-52996-x","article-title":"Biodiversity of mudflat intertidal viromes along the Chinese coasts","volume":"15","author":"Ji","year":"2024","journal-title":"Nat. Commun."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"1130","DOI":"10.1007\/s00343-023-3108-3","article-title":"Small temporal variation in abundance of virioplankton compared to bacterioplankton and phytoplankton in two bays in the northern South China Sea","volume":"42","author":"Zhang","year":"2024","journal-title":"J. Oceanol. Limnol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"e00122-11","DOI":"10.1128\/mBio.00122-11","article-title":"Phylogenetic Molecular Ecological Network of Soil Microbial Communities in Response to Elevated CO2","volume":"2","author":"Zhou","year":"2011","journal-title":"mBio"},{"key":"ref_62","doi-asserted-by":"crossref","unstructured":"Berry, D., and Widder, S. (2014). Deciphering microbial interactions and detecting keystone species with co-occurrence networks. Front. Microbiol., 5.","DOI":"10.3389\/fmicb.2014.00219"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"184","DOI":"10.1186\/s40168-024-01868-z","article-title":"Networks as tools for defining emergent properties of microbiomes and their stability","volume":"12","author":"Kajihara","year":"2024","journal-title":"Microbiome"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"e11707","DOI":"10.1002\/advs.202511707","article-title":"Diversity and Ecological Potentials of Marine Viruses Inhabiting Continental Shelf Seas","volume":"13","author":"Guo","year":"2025","journal-title":"Adv. Sci."},{"key":"ref_65","doi-asserted-by":"crossref","unstructured":"Heyerhoff, B., Engelen, B., and Bunse, C. (2022). Auxiliary Metabolic Gene Functions in Pelagic and Benthic Viruses of the Baltic Sea. Front. Microbiol., 13.","DOI":"10.3389\/fmicb.2022.863620"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"218","DOI":"10.1186\/s40168-024-01902-0","article-title":"Surface microlayer-mediated virome dissemination in the Central Arctic","volume":"12","author":"Rahlff","year":"2024","journal-title":"Microbiome"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"7547","DOI":"10.1128\/AEM.02229-13","article-title":"Bacteriophage Orphan DNA Methyltransferases: Insights from Their Bacterial Origin, Function, and Occurrence","volume":"79","author":"Murphy","year":"2013","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1038\/s43705-023-00249-1","article-title":"The association of prokaryotic antiviral systems and symbiotic phage communities in drinking water microbiomes","volume":"3","author":"Huang","year":"2023","journal-title":"ISME Commun."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"106271","DOI":"10.1016\/j.micpath.2023.106271","article-title":"Epigenetics regulation during virus-host interaction and their effects on the virus and host cell","volume":"182","author":"Rehman","year":"2023","journal-title":"Microb. Pathog."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"118","DOI":"10.1186\/s40168-023-01547-5","article-title":"Water mass age structures the auxiliary metabolic gene content of free-living and particle-attached deep ocean viral communities","volume":"11","author":"Coutinho","year":"2023","journal-title":"Microbiome"},{"key":"ref_71","first-page":"e00396-21","article-title":"Ecogenomics and Adaptation Strategies of Southern Ocean Viral Communities","volume":"6","author":"Diez","year":"2021","journal-title":"mSystems"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"122253","DOI":"10.1016\/j.watres.2024.122253","article-title":"Decrypting the viral community in aerobic activated sludge reactors treating antibiotic production wastewater","volume":"265","author":"Tang","year":"2024","journal-title":"Water Res."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1016\/j.molcel.2015.01.001","article-title":"An Ancient Riboswitch Class in Bacteria Regulates Purine Biosynthesis and One-Carbon Metabolism","volume":"57","author":"Kim","year":"2015","journal-title":"Mol. Cell"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"880","DOI":"10.1039\/C9MD00078J","article-title":"Revitalizing antifolates through understanding mechanisms that govern susceptibility and resistance","volume":"10","author":"Kordus","year":"2019","journal-title":"MedChemComm"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"128014","DOI":"10.1016\/j.micres.2024.128014","article-title":"Effects of folate biosynthesis defects in Lactiplantibacillus plantarum","volume":"292","author":"Cao","year":"2025","journal-title":"Microbiol. Res."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1186\/s40793-025-00779-2","article-title":"New insights into the evolution and metabolism of the bacterial phylum Candidatus Acidulodesulfobacteriota through metagenomics","volume":"20","author":"Ren","year":"2025","journal-title":"Environ. Microbiome"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1146\/annurev.micro.61.080706.093139","article-title":"As the worm turns: The earthworm gut as a transient habitat for soil microbial biomes","volume":"61","author":"Drake","year":"2007","journal-title":"Annu. Rev. Microbiol."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"1004","DOI":"10.1038\/s41396-023-01408-x","article-title":"Benzo a pyrene stress impacts adaptive strategies and ecological functions of earthworm intestinal viromes","volume":"17","author":"Xia","year":"2023","journal-title":"ISME J."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"1288","DOI":"10.1111\/j.1365-2958.2004.04767.x","article-title":"Evidence that WbpD is an N-acetyltransferase belonging to the hexapeptide acyltransferase superfamily and an important protein for O-antigen biosynthesis in Pseudomonas aeruginosa PAO1","volume":"57","author":"Wenzel","year":"2005","journal-title":"Mol. Microbiol."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"5446","DOI":"10.1021\/bi900186u","article-title":"Biosynthesis of UDP-GlcNAc(3NAc)A by WbpB, WbpE, and WbpD: Enzymes in the Wbp Pathway Responsible for O-Antigen Assembly in Pseudomonas aeruginosa PAO1","volume":"48","author":"Larkin","year":"2009","journal-title":"Biochemistry"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"5056","DOI":"10.1038\/srep05056","article-title":"Involvement of the Wbp pathway in the biosynthesis of Porphyromonas gingivalis lipopolysaccharide with anionic polysaccharide","volume":"4","author":"Shoji","year":"2014","journal-title":"Sci. Rep."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"e00893-17","DOI":"10.1128\/mBio.00893-17","article-title":"Deep-Sea Hydrothermal Vent Viruses Compensate for Microbial Metabolism in Virus-Host Interactions","volume":"8","author":"He","year":"2017","journal-title":"mBio"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1038\/nature04111","article-title":"Photosynthesis genes in marine viruses yield proteins during host infection","volume":"438","author":"Lindell","year":"2005","journal-title":"Nature"},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"3697","DOI":"10.1007\/s00018-009-0103-6","article-title":"Cyanobacterial psbA gene family: Optimization of oxygenic photosynthesis","volume":"66","author":"Mulo","year":"2009","journal-title":"Cell. Mol. Life Sci."},{"key":"ref_85","doi-asserted-by":"crossref","unstructured":"Bragg, J.G., and Chisholm, S.W. (2008). Modeling the Fitness Consequences of a Cyanophage-Encoded Photosynthesis Gene. PLoS ONE, 3.","DOI":"10.1371\/journal.pone.0003550"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"1273","DOI":"10.1038\/s41396-017-0043-3","article-title":"Energy limitation of cyanophage development: Implications for marine carbon cycling","volume":"12","author":"Puxty","year":"2018","journal-title":"ISME J."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"109471","DOI":"10.1016\/j.celrep.2021.109471","article-title":"Virus-associated organosulfur metabolism in human and environmental systems","volume":"36","author":"Kieft","year":"2021","journal-title":"Cell Rep."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"109773","DOI":"10.1016\/j.soilbio.2025.109773","article-title":"Potential viral influence on sulfur metabolism in acid sulfate soils","volume":"205","author":"Bi","year":"2025","journal-title":"Soil Biol. Biochem."},{"key":"ref_89","doi-asserted-by":"crossref","unstructured":"Abdelrahman, F., Easwaran, M., Daramola, O.I., Ragab, S., Lynch, S., Oduselu, T.J., Khan, F.M., Ayobami, A., Adnan, F., and Torrents, E. (2021). Phage-Encoded Endolysins. Antibiotics, 10.","DOI":"10.3390\/antibiotics10020124"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"463","DOI":"10.1007\/s10930-023-10139-z","article-title":"Bacteriophage Endolysin: A Powerful Weapon to Control Bacterial Biofilms","volume":"42","author":"Liu","year":"2023","journal-title":"Protein J."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"1320","DOI":"10.4319\/lo.2000.45.6.1320","article-title":"Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems","volume":"45","author":"Thingstad","year":"2000","journal-title":"Limnol. Oceanogr."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1128\/MMBR.64.1.69-114.2000","article-title":"Virioplankton: Viruses in aquatic ecosystems","volume":"64","author":"Wommack","year":"2000","journal-title":"Microbiol. Mol. Biol. Rev."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"871","DOI":"10.1016\/j.scib.2020.12.014","article-title":"Revisiting marine lytic and lysogenic virus-host interactions: Kill-the-Winner and Piggyback-the-Winner","volume":"66","author":"Chen","year":"2021","journal-title":"Sci. Bull."},{"key":"ref_94","doi-asserted-by":"crossref","unstructured":"Curtis-Harper, E., Pearson, V.K., Summers, S., Bridges, J.C., Schwenzer, S.P., and Olsson-Francis, K. (2018). The Microbial Community of a Terrestrial Anoxic Inter-Tidal Zone: A Model for Laboratory-Based Studies of Potentially Habitable Ancient Lacustrine Systems on Mars. Microorganisms, 6.","DOI":"10.3390\/microorganisms6030061"},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"L8","DOI":"10.3847\/2041-8213\/ade434","article-title":"Tides Tighten the Hycean Habitable Zone","volume":"987","author":"Livesey","year":"2025","journal-title":"Astrophys. J. Lett."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"967","DOI":"10.1089\/ast.2017.1718","article-title":"Implications of Tides for Life on Exoplanets","volume":"18","author":"Lingam","year":"2018","journal-title":"Astrobiology"},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"wraf198","DOI":"10.1093\/ismejo\/wraf198","article-title":"Multiple roles of DNA methylation in sea-ice bacterial communities and associated viruses","volume":"19","author":"Kanaan","year":"2025","journal-title":"ISME J."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1007\/s00792-026-01426-5","article-title":"Extreme Arabian environments and their microbiomes: New frontiers for astrobiology and biosignature discovery","volume":"30","author":"Schultz","year":"2026","journal-title":"Extremophiles"}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/18\/5\/500\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,4,29]],"date-time":"2026-04-29T07:47:59Z","timestamp":1777448879000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/18\/5\/500"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,4,25]]},"references-count":98,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2026,5]]}},"alternative-id":["v18050500"],"URL":"https:\/\/doi.org\/10.3390\/v18050500","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,4,25]]}}}