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      A Novel Phage Infecting Alteromonas Represents a Distinct Group of Siphophages Infecting Diverse Aquatic Copiotrophs

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          ABSTRACT

          Bacteriophages play critical roles in impacting microbial community succession both ecologically and evolutionarily. Although the majority of phage genetic diversity has been increasingly unveiled, phages infecting members of the ecologically important genus Alteromonas remain poorly understood. Here, we present a comprehensive analysis of a newly isolated alterophage, vB_AcoS-R7M (R7M), to characterize its life cycle traits, genomic features, and putative evolutionary origin. R7M harbors abundant genes identified as host-like auxiliary metabolic genes facilitating viral propagation. Genomic analysis suggested that R7M is distinct from currently known alterophages. Interestingly, R7M was found to share a set of similar characteristics with a number of siphophages infecting diverse aquatic opportunistic copiotrophs. We therefore proposed the creation of one new subfamily ( Queuovirinae) to group with these evolutionarily related phages. Notably, tail genes were less likely to be shared among them, and baseplate-related genes varied the most. In-depth analyses indicated that R7M has replaced its distal tail with a Rhodobacter capsulatus gene transfer agent (RcGTA)-like baseplate and further acquired a putative receptor interaction site targeting Alteromonas. These findings suggest that horizontal exchanges of viral tail adsorption apparatuses are widespread and vital for phages to hunt new hosts and to adapt to new niches.

          IMPORTANCE The evolution and ecology of phages infecting members of Alteromonas, a marine opportunistic genus that is widely distributed and of great ecological significance, remain poorly understood. The present study integrates physiological and genomic evidence to characterize the properties and putative phage-host interactions of a newly isolated Alteromonas phage, vB_AcoS-R7M (R7M). A taxonomic study reveals close evolutionary relationships among R7M and a number of siphophages infecting various aquatic copiotrophs. Their similar head morphology and overall genetic framework suggest their putative common ancestry and the grouping of a new viral subfamily. However, their major difference lies in the viral tail adsorption apparatuses and the horizontal exchanges of which possibly account for variations in host specificity. These findings outline an evolutionary scenario for the emergence of diverse viral lineages of a shared genetic pool and give insights into the genetics and ecology of viral host jumps.

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            MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets.

            We present the latest version of the Molecular Evolutionary Genetics Analysis (Mega) software, which contains many sophisticated methods and tools for phylogenomics and phylomedicine. In this major upgrade, Mega has been optimized for use on 64-bit computing systems for analyzing larger datasets. Researchers can now explore and analyze tens of thousands of sequences in Mega The new version also provides an advanced wizard for building timetrees and includes a new functionality to automatically predict gene duplication events in gene family trees. The 64-bit Mega is made available in two interfaces: graphical and command line. The graphical user interface (GUI) is a native Microsoft Windows application that can also be used on Mac OS X. The command line Mega is available as native applications for Windows, Linux, and Mac OS X. They are intended for use in high-throughput and scripted analysis. Both versions are available from www.megasoftware.net free of charge.
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              IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era

              Abstract IQ-TREE (http://www.iqtree.org, last accessed February 6, 2020) is a user-friendly and widely used software package for phylogenetic inference using maximum likelihood. Since the release of version 1 in 2014, we have continuously expanded IQ-TREE to integrate a plethora of new models of sequence evolution and efficient computational approaches of phylogenetic inference to deal with genomic data. Here, we describe notable features of IQ-TREE version 2 and highlight the key advantages over other software.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                mSphere
                mSphere
                msphere
                mSphere
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                2379-5042
                9 June 2021
                May-Jun 2021
                9 June 2021
                : 6
                : 3
                : e00454-21
                Affiliations
                [a ]State Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Institute of Marine Microbes and Ecospheres, Xiamen University, Xiamen, China
                [b ]College of Ocean and Earth Sciences, Xiamen University, Xiamen, China
                [c ]Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Zhuhai, China
                University of Iowa
                Author notes

                Citation Ma R, Lai J, Chen X, Wang L, Yang Y, Wei S, Jiao N, Zhang R. 2021. A novel phage infecting Alteromonas represents a distinct group of siphophages infecting diverse aquatic copiotrophs. mSphere 6:e00454-21. https://doi.org/10.1128/mSphere.00454-21.

                Article
                mSphere00454-21
                10.1128/mSphere.00454-21
                8265664
                34106770
                89e0e499-3ae5-447f-b567-c67d4814ad70
                Copyright © 2021 Ma et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                History
                : 17 May 2021
                : 19 May 2021
                Page count
                supplementary-material: 8, Figures: 6, Tables: 1, Equations: 0, References: 72, Pages: 16, Words: 9646
                Funding
                Funded by: Bureau of Science and Information Technology of Guangzhou Municipality | Guangzhou Science and Technology Program key projects, FundRef https://doi.org/10.13039/501100004000;
                Award ID: 201904020029
                Award Recipient :
                Funded by: China Ocean Mineral Resources Research and Development Association (COMRA), FundRef https://doi.org/10.13039/501100010823;
                Award ID: DY135-E2-1-04
                Award Recipient :
                Funded by: MOE | Fundamental Research Funds for the Central Universities (Fundamental Research Fund for the Central Universities), FundRef https://doi.org/10.13039/501100012226;
                Award ID: 20720200027
                Award Recipient :
                Funded by: MOE | Fundamental Research Funds for the Central Universities (Fundamental Research Fund for the Central Universities), FundRef https://doi.org/10.13039/501100012226;
                Award ID: 20720170107
                Award Recipient :
                Funded by: National Natural Science Foundation of China (NSFC), FundRef https://doi.org/10.13039/501100001809;
                Award ID: 91951209
                Award Recipient :
                Funded by: National Natural Science Foundation of China (NSFC), FundRef https://doi.org/10.13039/501100001809;
                Award ID: 41861144018
                Award Recipient :
                Categories
                Research Article
                bacteriophages, Bacteriophages
                Custom metadata
                May/June 2021

                bacteriophage,alteromonas,auxiliary metabolic genes,comparative genomic analysis,phage taxonomy,receptor binding protein

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