CRISPR Spacers Indicate Preferential Matching of Specific Virioplankton Genes

ABSTRACT Viral infection exerts selection pressure on marine microbes, as virus-induced cell lysis causes 20 to 50% of cell mortality, resulting in fluxes of biomass into oceanic dissolved organic matter. Archaeal and bacterial populations can defend against viral infection using the clustered regul...

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Autores principales:	Daniel J. Nasko, Barbra D. Ferrell, Ryan M. Moore, Jaysheel D. Bhavsar, Shawn W. Polson, K. Eric Wommack
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	bacteriophage biogeography bioinformatics metagenomics oceanography viral ecology Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/a013f19c7de0412a8a6bf4826132e2a1
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spelling	oai:doaj.org-article:a013f19c7de0412a8a6bf4826132e2a12021-11-15T15:55:24ZCRISPR Spacers Indicate Preferential Matching of Specific Virioplankton Genes10.1128/mBio.02651-182150-7511https://doaj.org/article/a013f19c7de0412a8a6bf4826132e2a12019-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02651-18https://doaj.org/toc/2150-7511ABSTRACT Viral infection exerts selection pressure on marine microbes, as virus-induced cell lysis causes 20 to 50% of cell mortality, resulting in fluxes of biomass into oceanic dissolved organic matter. Archaeal and bacterial populations can defend against viral infection using the clustered regularly interspaced short palindromic repeat (CRISPR)-associated (Cas) system, which relies on specific matching between a spacer sequence and a viral gene. If a CRISPR spacer match to any gene within a viral genome is equally effective in preventing lysis, no viral genes should be preferentially matched by CRISPR spacers. However, if there are differences in effectiveness, certain viral genes may demonstrate a greater frequency of CRISPR spacer matches. Indeed, homology search analyses of bacterioplankton CRISPR spacer sequences against virioplankton sequences revealed preferential matching of replication proteins, nucleic acid binding proteins, and viral structural proteins. Positive selection pressure for effective viral defense is one parsimonious explanation for these observations. CRISPR spacers from virioplankton metagenomes preferentially matched methyltransferase and phage integrase genes within virioplankton sequences. These virioplankton CRISPR spacers may assist infected host cells in defending against competing phage. Analyses also revealed that half of the spacer-matched viral genes were unknown, some genes matched several spacers, and some spacers matched multiple genes, a many-to-many relationship. Thus, CRISPR spacer matching may be an evolutionary algorithm, agnostically identifying those genes under stringent selection pressure for sustaining viral infection and lysis. Investigating this subset of viral genes could reveal those genetic mechanisms essential to virus-host interactions and provide new technologies for optimizing CRISPR defense in beneficial microbes. IMPORTANCE The CRISPR-Cas system is one means by which bacterial and archaeal populations defend against viral infection which causes 20 to 50% of cell mortality in the ocean. We tested the hypothesis that certain viral genes are preferentially targeted for the initial attack of the CRISPR-Cas system on a viral genome. Using CASC, a pipeline for CRISPR spacer discovery, and metagenome data from oceanic microbes and viruses, we found a clear subset of viral genes with high match frequencies to CRISPR spacers. Moreover, we observed a many-to-many relationship of spacers and viral genes. These high-match viral genes were involved in nucleotide metabolism, DNA methylation, and viral structure. It is possible that CRISPR spacer matching is an evolutionary algorithm pointing to those viral genes most important to sustaining infection and lysis. Studying these genes may advance the understanding of virus-host interactions in nature and provide new technologies for leveraging CRISPR-Cas systems in beneficial microbes.Daniel J. NaskoBarbra D. FerrellRyan M. MooreJaysheel D. BhavsarShawn W. PolsonK. Eric WommackAmerican Society for Microbiologyarticlebacteriophagebiogeographybioinformaticsmetagenomicsoceanographyviral ecologyMicrobiologyQR1-502ENmBio, Vol 10, Iss 2 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	bacteriophage biogeography bioinformatics metagenomics oceanography viral ecology Microbiology QR1-502
spellingShingle	bacteriophage biogeography bioinformatics metagenomics oceanography viral ecology Microbiology QR1-502 Daniel J. Nasko Barbra D. Ferrell Ryan M. Moore Jaysheel D. Bhavsar Shawn W. Polson K. Eric Wommack CRISPR Spacers Indicate Preferential Matching of Specific Virioplankton Genes
description	ABSTRACT Viral infection exerts selection pressure on marine microbes, as virus-induced cell lysis causes 20 to 50% of cell mortality, resulting in fluxes of biomass into oceanic dissolved organic matter. Archaeal and bacterial populations can defend against viral infection using the clustered regularly interspaced short palindromic repeat (CRISPR)-associated (Cas) system, which relies on specific matching between a spacer sequence and a viral gene. If a CRISPR spacer match to any gene within a viral genome is equally effective in preventing lysis, no viral genes should be preferentially matched by CRISPR spacers. However, if there are differences in effectiveness, certain viral genes may demonstrate a greater frequency of CRISPR spacer matches. Indeed, homology search analyses of bacterioplankton CRISPR spacer sequences against virioplankton sequences revealed preferential matching of replication proteins, nucleic acid binding proteins, and viral structural proteins. Positive selection pressure for effective viral defense is one parsimonious explanation for these observations. CRISPR spacers from virioplankton metagenomes preferentially matched methyltransferase and phage integrase genes within virioplankton sequences. These virioplankton CRISPR spacers may assist infected host cells in defending against competing phage. Analyses also revealed that half of the spacer-matched viral genes were unknown, some genes matched several spacers, and some spacers matched multiple genes, a many-to-many relationship. Thus, CRISPR spacer matching may be an evolutionary algorithm, agnostically identifying those genes under stringent selection pressure for sustaining viral infection and lysis. Investigating this subset of viral genes could reveal those genetic mechanisms essential to virus-host interactions and provide new technologies for optimizing CRISPR defense in beneficial microbes. IMPORTANCE The CRISPR-Cas system is one means by which bacterial and archaeal populations defend against viral infection which causes 20 to 50% of cell mortality in the ocean. We tested the hypothesis that certain viral genes are preferentially targeted for the initial attack of the CRISPR-Cas system on a viral genome. Using CASC, a pipeline for CRISPR spacer discovery, and metagenome data from oceanic microbes and viruses, we found a clear subset of viral genes with high match frequencies to CRISPR spacers. Moreover, we observed a many-to-many relationship of spacers and viral genes. These high-match viral genes were involved in nucleotide metabolism, DNA methylation, and viral structure. It is possible that CRISPR spacer matching is an evolutionary algorithm pointing to those viral genes most important to sustaining infection and lysis. Studying these genes may advance the understanding of virus-host interactions in nature and provide new technologies for leveraging CRISPR-Cas systems in beneficial microbes.
format	article
author	Daniel J. Nasko Barbra D. Ferrell Ryan M. Moore Jaysheel D. Bhavsar Shawn W. Polson K. Eric Wommack
author_facet	Daniel J. Nasko Barbra D. Ferrell Ryan M. Moore Jaysheel D. Bhavsar Shawn W. Polson K. Eric Wommack
author_sort	Daniel J. Nasko
title	CRISPR Spacers Indicate Preferential Matching of Specific Virioplankton Genes
title_short	CRISPR Spacers Indicate Preferential Matching of Specific Virioplankton Genes
title_full	CRISPR Spacers Indicate Preferential Matching of Specific Virioplankton Genes
title_fullStr	CRISPR Spacers Indicate Preferential Matching of Specific Virioplankton Genes
title_full_unstemmed	CRISPR Spacers Indicate Preferential Matching of Specific Virioplankton Genes
title_sort	crispr spacers indicate preferential matching of specific virioplankton genes
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/a013f19c7de0412a8a6bf4826132e2a1
work_keys_str_mv	AT danieljnasko crisprspacersindicatepreferentialmatchingofspecificvirioplanktongenes AT barbradferrell crisprspacersindicatepreferentialmatchingofspecificvirioplanktongenes AT ryanmmoore crisprspacersindicatepreferentialmatchingofspecificvirioplanktongenes AT jaysheeldbhavsar crisprspacersindicatepreferentialmatchingofspecificvirioplanktongenes AT shawnwpolson crisprspacersindicatepreferentialmatchingofspecificvirioplanktongenes AT kericwommack crisprspacersindicatepreferentialmatchingofspecificvirioplanktongenes
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CRISPR Spacers Indicate Preferential Matching of Specific Virioplankton Genes

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