Orphan Genes Shared by Pathogenic Genomes Are More Associated with Bacterial Pathogenicity

ABSTRACT Orphan genes (also known as ORFans [i.e., orphan open reading frames]) are new genes that enable an organism to adapt to its specific living environment. Our focus in this study is to compare ORFans between pathogens (P) and nonpathogens (NP) of the same genus. Using the pangenome idea, we...

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Autores principales:	Sarah Entwistle, Xueqiong Li, Yanbin Yin
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	ORFan orphan gene horizontal gene transfer pathogenic island pathogenicity prophage Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/810af41a16e74ffc85ab6f3c478fa7e8
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spelling	oai:doaj.org-article:810af41a16e74ffc85ab6f3c478fa7e82021-12-02T18:39:15ZOrphan Genes Shared by Pathogenic Genomes Are More Associated with Bacterial Pathogenicity10.1128/mSystems.00290-182379-5077https://doaj.org/article/810af41a16e74ffc85ab6f3c478fa7e82019-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00290-18https://doaj.org/toc/2379-5077ABSTRACT Orphan genes (also known as ORFans [i.e., orphan open reading frames]) are new genes that enable an organism to adapt to its specific living environment. Our focus in this study is to compare ORFans between pathogens (P) and nonpathogens (NP) of the same genus. Using the pangenome idea, we have identified 130,169 ORFans in nine bacterial genera (505 genomes) and classified these ORFans into four groups: (i) SS-ORFans (P), which are only found in a single pathogenic genome; (ii) SS-ORFans (NP), which are only found in a single nonpathogenic genome; (iii) PS-ORFans (P), which are found in multiple pathogenic genomes; and (iv) NS-ORFans (NP), which are found in multiple nonpathogenic genomes. Within the same genus, pathogens do not always have more genes, more ORFans, or more pathogenicity-related genes (PRGs)—including prophages, pathogenicity islands (PAIs), virulence factors (VFs), and horizontal gene transfers (HGTs)—than nonpathogens. Interestingly, in pathogens of the nine genera, the percentages of PS-ORFans are consistently higher than those of SS-ORFans, which is not true in nonpathogens. Similarly, in pathogens of the nine genera, the percentages of PS-ORFans matching the four types of PRGs are also always higher than those of SS-ORFans, but this is not true in nonpathogens. All of these findings suggest the greater importance of PS-ORFans for bacterial pathogenicity. IMPORTANCE Recent pangenome analyses of numerous bacterial species have suggested that each genome of a single species may have a significant fraction of its gene content unique or shared by a very few genomes (i.e., ORFans). We selected nine bacterial genera, each containing at least five pathogenic and five nonpathogenic genomes, to compare their ORFans in relation to pathogenicity-related genes. Pathogens in these genera are known to cause a number of common and devastating human diseases such as pneumonia, diphtheria, melioidosis, and tuberculosis. Thus, they are worthy of in-depth systems microbiology investigations, including the comparative study of ORFans between pathogens and nonpathogens. We provide direct evidence to suggest that ORFans shared by more pathogens are more associated with pathogenicity-related genes and thus are more important targets for development of new diagnostic markers or therapeutic drugs for bacterial infectious diseases.Sarah EntwistleXueqiong LiYanbin YinAmerican Society for MicrobiologyarticleORFanorphan genehorizontal gene transferpathogenic islandpathogenicityprophageMicrobiologyQR1-502ENmSystems, Vol 4, Iss 1 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	ORFan orphan gene horizontal gene transfer pathogenic island pathogenicity prophage Microbiology QR1-502
spellingShingle	ORFan orphan gene horizontal gene transfer pathogenic island pathogenicity prophage Microbiology QR1-502 Sarah Entwistle Xueqiong Li Yanbin Yin Orphan Genes Shared by Pathogenic Genomes Are More Associated with Bacterial Pathogenicity
description	ABSTRACT Orphan genes (also known as ORFans [i.e., orphan open reading frames]) are new genes that enable an organism to adapt to its specific living environment. Our focus in this study is to compare ORFans between pathogens (P) and nonpathogens (NP) of the same genus. Using the pangenome idea, we have identified 130,169 ORFans in nine bacterial genera (505 genomes) and classified these ORFans into four groups: (i) SS-ORFans (P), which are only found in a single pathogenic genome; (ii) SS-ORFans (NP), which are only found in a single nonpathogenic genome; (iii) PS-ORFans (P), which are found in multiple pathogenic genomes; and (iv) NS-ORFans (NP), which are found in multiple nonpathogenic genomes. Within the same genus, pathogens do not always have more genes, more ORFans, or more pathogenicity-related genes (PRGs)—including prophages, pathogenicity islands (PAIs), virulence factors (VFs), and horizontal gene transfers (HGTs)—than nonpathogens. Interestingly, in pathogens of the nine genera, the percentages of PS-ORFans are consistently higher than those of SS-ORFans, which is not true in nonpathogens. Similarly, in pathogens of the nine genera, the percentages of PS-ORFans matching the four types of PRGs are also always higher than those of SS-ORFans, but this is not true in nonpathogens. All of these findings suggest the greater importance of PS-ORFans for bacterial pathogenicity. IMPORTANCE Recent pangenome analyses of numerous bacterial species have suggested that each genome of a single species may have a significant fraction of its gene content unique or shared by a very few genomes (i.e., ORFans). We selected nine bacterial genera, each containing at least five pathogenic and five nonpathogenic genomes, to compare their ORFans in relation to pathogenicity-related genes. Pathogens in these genera are known to cause a number of common and devastating human diseases such as pneumonia, diphtheria, melioidosis, and tuberculosis. Thus, they are worthy of in-depth systems microbiology investigations, including the comparative study of ORFans between pathogens and nonpathogens. We provide direct evidence to suggest that ORFans shared by more pathogens are more associated with pathogenicity-related genes and thus are more important targets for development of new diagnostic markers or therapeutic drugs for bacterial infectious diseases.
format	article
author	Sarah Entwistle Xueqiong Li Yanbin Yin
author_facet	Sarah Entwistle Xueqiong Li Yanbin Yin
author_sort	Sarah Entwistle
title	Orphan Genes Shared by Pathogenic Genomes Are More Associated with Bacterial Pathogenicity
title_short	Orphan Genes Shared by Pathogenic Genomes Are More Associated with Bacterial Pathogenicity
title_full	Orphan Genes Shared by Pathogenic Genomes Are More Associated with Bacterial Pathogenicity
title_fullStr	Orphan Genes Shared by Pathogenic Genomes Are More Associated with Bacterial Pathogenicity
title_full_unstemmed	Orphan Genes Shared by Pathogenic Genomes Are More Associated with Bacterial Pathogenicity
title_sort	orphan genes shared by pathogenic genomes are more associated with bacterial pathogenicity
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/810af41a16e74ffc85ab6f3c478fa7e8
work_keys_str_mv	AT sarahentwistle orphangenessharedbypathogenicgenomesaremoreassociatedwithbacterialpathogenicity AT xueqiongli orphangenessharedbypathogenicgenomesaremoreassociatedwithbacterialpathogenicity AT yanbinyin orphangenessharedbypathogenicgenomesaremoreassociatedwithbacterialpathogenicity
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Orphan Genes Shared by Pathogenic Genomes Are More Associated with Bacterial Pathogenicity

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