Antimicrobial Peptides, Polymorphic Toxins, and Self-Nonself Recognition Systems in Archaea: an Untapped Armory for Intermicrobial Conflicts

ABSTRACT Numerous, diverse, highly variable defense and offense genetic systems are encoded in most bacterial genomes and are involved in various forms of conflict among competing microbes or their eukaryotic hosts. Here we focus on the offense and self-versus-nonself discrimination systems encoded...

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Autores principales:	Kira S. Makarova, Yuri I. Wolf, Svetlana Karamycheva, Dapeng Zhang, L. Aravind, Eugene V. Koonin
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	archaea archaeocins polymorphic toxins quorum sensing Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/24ac9e7b6ea14842b22fbe4432cff67a
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spelling	oai:doaj.org-article:24ac9e7b6ea14842b22fbe4432cff67a2021-11-15T15:55:24ZAntimicrobial Peptides, Polymorphic Toxins, and Self-Nonself Recognition Systems in Archaea: an Untapped Armory for Intermicrobial Conflicts10.1128/mBio.00715-192150-7511https://doaj.org/article/24ac9e7b6ea14842b22fbe4432cff67a2019-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00715-19https://doaj.org/toc/2150-7511ABSTRACT Numerous, diverse, highly variable defense and offense genetic systems are encoded in most bacterial genomes and are involved in various forms of conflict among competing microbes or their eukaryotic hosts. Here we focus on the offense and self-versus-nonself discrimination systems encoded by archaeal genomes that so far have remained largely uncharacterized and unannotated. Specifically, we analyze archaeal genomic loci encoding polymorphic and related toxin systems and ribosomally synthesized antimicrobial peptides. Using sensitive methods for sequence comparison and the “guilt by association” approach, we identified such systems in 141 archaeal genomes. These toxins can be classified into four major groups based on the structure of the components involved in the toxin delivery. The toxin domains are often shared between and within each system. We revisit halocin families and substantially expand the halocin C8 family, which was identified in diverse archaeal genomes and also certain bacteria. Finally, we employ features of protein sequences and genomic locus organization characteristic of archaeocins and polymorphic toxins to identify candidates for analogous but not necessarily homologous systems among uncharacterized protein families. This work confidently predicts that more than 1,600 archaeal proteins, currently annotated as “hypothetical” in public databases, are components of conflict and self-versus-nonself discrimination systems. IMPORTANCE Diverse and highly variable systems involved in biological conflicts and self-versus-nonself discrimination are ubiquitous in bacteria but much less studied in archaea. We performed comprehensive comparative genomic analyses of the archaeal systems that share components with analogous bacterial systems and propose an approach to identify new systems that could be involved in these functions. We predict polymorphic toxin systems in 141 archaeal genomes and identify new, archaea-specific toxin and immunity protein families. These systems are widely represented in archaea and are predicted to play major roles in interactions between species and in intermicrobial conflicts. This work is expected to stimulate experimental research to advance the understanding of poorly characterized major aspects of archaeal biology.Kira S. MakarovaYuri I. WolfSvetlana KaramychevaDapeng ZhangL. AravindEugene V. KooninAmerican Society for Microbiologyarticlearchaeaarchaeocinspolymorphic toxinsquorum sensingMicrobiologyQR1-502ENmBio, Vol 10, Iss 3 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	archaea archaeocins polymorphic toxins quorum sensing Microbiology QR1-502
spellingShingle	archaea archaeocins polymorphic toxins quorum sensing Microbiology QR1-502 Kira S. Makarova Yuri I. Wolf Svetlana Karamycheva Dapeng Zhang L. Aravind Eugene V. Koonin Antimicrobial Peptides, Polymorphic Toxins, and Self-Nonself Recognition Systems in Archaea: an Untapped Armory for Intermicrobial Conflicts
description	ABSTRACT Numerous, diverse, highly variable defense and offense genetic systems are encoded in most bacterial genomes and are involved in various forms of conflict among competing microbes or their eukaryotic hosts. Here we focus on the offense and self-versus-nonself discrimination systems encoded by archaeal genomes that so far have remained largely uncharacterized and unannotated. Specifically, we analyze archaeal genomic loci encoding polymorphic and related toxin systems and ribosomally synthesized antimicrobial peptides. Using sensitive methods for sequence comparison and the “guilt by association” approach, we identified such systems in 141 archaeal genomes. These toxins can be classified into four major groups based on the structure of the components involved in the toxin delivery. The toxin domains are often shared between and within each system. We revisit halocin families and substantially expand the halocin C8 family, which was identified in diverse archaeal genomes and also certain bacteria. Finally, we employ features of protein sequences and genomic locus organization characteristic of archaeocins and polymorphic toxins to identify candidates for analogous but not necessarily homologous systems among uncharacterized protein families. This work confidently predicts that more than 1,600 archaeal proteins, currently annotated as “hypothetical” in public databases, are components of conflict and self-versus-nonself discrimination systems. IMPORTANCE Diverse and highly variable systems involved in biological conflicts and self-versus-nonself discrimination are ubiquitous in bacteria but much less studied in archaea. We performed comprehensive comparative genomic analyses of the archaeal systems that share components with analogous bacterial systems and propose an approach to identify new systems that could be involved in these functions. We predict polymorphic toxin systems in 141 archaeal genomes and identify new, archaea-specific toxin and immunity protein families. These systems are widely represented in archaea and are predicted to play major roles in interactions between species and in intermicrobial conflicts. This work is expected to stimulate experimental research to advance the understanding of poorly characterized major aspects of archaeal biology.
format	article
author	Kira S. Makarova Yuri I. Wolf Svetlana Karamycheva Dapeng Zhang L. Aravind Eugene V. Koonin
author_facet	Kira S. Makarova Yuri I. Wolf Svetlana Karamycheva Dapeng Zhang L. Aravind Eugene V. Koonin
author_sort	Kira S. Makarova
title	Antimicrobial Peptides, Polymorphic Toxins, and Self-Nonself Recognition Systems in Archaea: an Untapped Armory for Intermicrobial Conflicts
title_short	Antimicrobial Peptides, Polymorphic Toxins, and Self-Nonself Recognition Systems in Archaea: an Untapped Armory for Intermicrobial Conflicts
title_full	Antimicrobial Peptides, Polymorphic Toxins, and Self-Nonself Recognition Systems in Archaea: an Untapped Armory for Intermicrobial Conflicts
title_fullStr	Antimicrobial Peptides, Polymorphic Toxins, and Self-Nonself Recognition Systems in Archaea: an Untapped Armory for Intermicrobial Conflicts
title_full_unstemmed	Antimicrobial Peptides, Polymorphic Toxins, and Self-Nonself Recognition Systems in Archaea: an Untapped Armory for Intermicrobial Conflicts
title_sort	antimicrobial peptides, polymorphic toxins, and self-nonself recognition systems in archaea: an untapped armory for intermicrobial conflicts
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/24ac9e7b6ea14842b22fbe4432cff67a
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Antimicrobial Peptides, Polymorphic Toxins, and Self-Nonself Recognition Systems in Archaea: an Untapped Armory for Intermicrobial Conflicts

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