Genomes of the “<italic toggle="yes">Candidatus</italic> Actinomarinales” Order: Highly Streamlined Marine Epipelagic Actinobacteria

ABSTRACT “Candidatus Actinomarinales” was defined as a subclass of exclusively marine Actinobacteria with small cells and genomes. We have collected all the available genomes in databases to assess the diversity included in this group and analyzed it by comparative genomics. We have found the equiva...

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Autores principales:	Mario López-Pérez, Jose M. Haro-Moreno, Jaime Iranzo, Francisco Rodriguez-Valera
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Actinomarinales single-amplified genomes marine Actinobacteria streamlined genomes Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/c79cd368388247d2bf10e793366458b7
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spelling	oai:doaj.org-article:c79cd368388247d2bf10e793366458b72021-12-02T19:46:19ZGenomes of the “<italic toggle="yes">Candidatus</italic> Actinomarinales” Order: Highly Streamlined Marine Epipelagic Actinobacteria10.1128/mSystems.01041-202379-5077https://doaj.org/article/c79cd368388247d2bf10e793366458b72020-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.01041-20https://doaj.org/toc/2379-5077ABSTRACT “Candidatus Actinomarinales” was defined as a subclass of exclusively marine Actinobacteria with small cells and genomes. We have collected all the available genomes in databases to assess the diversity included in this group and analyzed it by comparative genomics. We have found the equivalent of five genera and 18 genomospecies. They have genome reduction parameters equal to those of freshwater actinobacterial “Candidatus Nanopelagicales” or marine alphaproteobacterial Pelagibacterales. Genome recruitment shows that they are found only in the photic zone and mainly in surface waters, with only one genus that is found preferentially at or below the deep chlorophyll maximum. “Ca. Actinomarinales” show a highly conserved core genome (80% of the gene families conserved for the whole order) with a saturation of genomic diversity of the flexible genome at the genomospecies level. We found only a flexible genomic island preserved throughout the order; it is related to the sugar decoration of the envelope and uses several tRNAs as hot spots to increase its genomic diversity. Populations had a discrete level of sequence diversity similar to other marine microbes but drastically different from the much higher levels found for Pelagibacterales. Genomic analysis suggests that they are all aerobic photoheterotrophs with one type 1 rhodopsin and a heliorhodopsin. Like other actinobacteria, they possess the F420 coenzyme biosynthesis pathway, and its lower reduction potential could provide access to an increased range of redox chemical transformations. Last, sequence analysis revealed the first “Ca. Actinomarinales” phages, including a prophage, with metaviromic islands related to sialic acid cleavage. IMPORTANCE Microbiology is in a new age in which sequence databases are primary sources of information about many microbes. However, in-depth analysis of environmental genomes thus retrieved is essential to substantiate the new knowledge. Here, we study 182 genomes belonging to the only known exclusively marine pelagic group of the phylum Actinobacteria. The aquatic branch of this phylum is largely known from environmental sequencing studies (single-amplified genomes [SAGs] and metagenome-assembled genomes [MAGs]), and we have collected and analyzed the available information present in databases about the “Ca. Actinomarinales.” They are among the most streamlined microbes to live in the epipelagic zone of the ocean, and their study is critical to obtain a proper view of the diversity of Actinobacteria and their role in aquatic ecosystems.Mario López-PérezJose M. Haro-MorenoJaime IranzoFrancisco Rodriguez-ValeraAmerican Society for MicrobiologyarticleActinomarinalessingle-amplified genomesmarine Actinobacteriastreamlined genomesMicrobiologyQR1-502ENmSystems, Vol 5, Iss 6 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Actinomarinales single-amplified genomes marine Actinobacteria streamlined genomes Microbiology QR1-502
spellingShingle	Actinomarinales single-amplified genomes marine Actinobacteria streamlined genomes Microbiology QR1-502 Mario López-Pérez Jose M. Haro-Moreno Jaime Iranzo Francisco Rodriguez-Valera Genomes of the “<italic toggle="yes">Candidatus</italic> Actinomarinales” Order: Highly Streamlined Marine Epipelagic Actinobacteria
description	ABSTRACT “Candidatus Actinomarinales” was defined as a subclass of exclusively marine Actinobacteria with small cells and genomes. We have collected all the available genomes in databases to assess the diversity included in this group and analyzed it by comparative genomics. We have found the equivalent of five genera and 18 genomospecies. They have genome reduction parameters equal to those of freshwater actinobacterial “Candidatus Nanopelagicales” or marine alphaproteobacterial Pelagibacterales. Genome recruitment shows that they are found only in the photic zone and mainly in surface waters, with only one genus that is found preferentially at or below the deep chlorophyll maximum. “Ca. Actinomarinales” show a highly conserved core genome (80% of the gene families conserved for the whole order) with a saturation of genomic diversity of the flexible genome at the genomospecies level. We found only a flexible genomic island preserved throughout the order; it is related to the sugar decoration of the envelope and uses several tRNAs as hot spots to increase its genomic diversity. Populations had a discrete level of sequence diversity similar to other marine microbes but drastically different from the much higher levels found for Pelagibacterales. Genomic analysis suggests that they are all aerobic photoheterotrophs with one type 1 rhodopsin and a heliorhodopsin. Like other actinobacteria, they possess the F420 coenzyme biosynthesis pathway, and its lower reduction potential could provide access to an increased range of redox chemical transformations. Last, sequence analysis revealed the first “Ca. Actinomarinales” phages, including a prophage, with metaviromic islands related to sialic acid cleavage. IMPORTANCE Microbiology is in a new age in which sequence databases are primary sources of information about many microbes. However, in-depth analysis of environmental genomes thus retrieved is essential to substantiate the new knowledge. Here, we study 182 genomes belonging to the only known exclusively marine pelagic group of the phylum Actinobacteria. The aquatic branch of this phylum is largely known from environmental sequencing studies (single-amplified genomes [SAGs] and metagenome-assembled genomes [MAGs]), and we have collected and analyzed the available information present in databases about the “Ca. Actinomarinales.” They are among the most streamlined microbes to live in the epipelagic zone of the ocean, and their study is critical to obtain a proper view of the diversity of Actinobacteria and their role in aquatic ecosystems.
format	article
author	Mario López-Pérez Jose M. Haro-Moreno Jaime Iranzo Francisco Rodriguez-Valera
author_facet	Mario López-Pérez Jose M. Haro-Moreno Jaime Iranzo Francisco Rodriguez-Valera
author_sort	Mario López-Pérez
title	Genomes of the “<italic toggle="yes">Candidatus</italic> Actinomarinales” Order: Highly Streamlined Marine Epipelagic Actinobacteria
title_short	Genomes of the “<italic toggle="yes">Candidatus</italic> Actinomarinales” Order: Highly Streamlined Marine Epipelagic Actinobacteria
title_full	Genomes of the “<italic toggle="yes">Candidatus</italic> Actinomarinales” Order: Highly Streamlined Marine Epipelagic Actinobacteria
title_fullStr	Genomes of the “<italic toggle="yes">Candidatus</italic> Actinomarinales” Order: Highly Streamlined Marine Epipelagic Actinobacteria
title_full_unstemmed	Genomes of the “<italic toggle="yes">Candidatus</italic> Actinomarinales” Order: Highly Streamlined Marine Epipelagic Actinobacteria
title_sort	genomes of the “<italic toggle="yes">candidatus</italic> actinomarinales” order: highly streamlined marine epipelagic actinobacteria
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/c79cd368388247d2bf10e793366458b7
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Genomes of the “<italic toggle="yes">Candidatus</italic> Actinomarinales” Order: Highly Streamlined Marine Epipelagic Actinobacteria

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