Cargando…

Comparative Genomics Highlights Symbiotic Capacities and High Metabolic Flexibility of the Marine Genus Pseudovibrio

Pseudovibrio is a marine bacterial genus members of which are predominantly isolated from sessile marine animals, and particularly sponges. It has been hypothesized that Pseudovibrio spp. form mutualistic relationships with their hosts. Here, we studied Pseudovibrio phylogeny and genetic adaptations...

Descripción completa

Detalles Bibliográficos
Autores principales: Versluis, Dennis, Nijsse, Bart, Naim, Mohd Azrul, Koehorst, Jasper J, Wiese, Jutta, Imhoff, Johannes F, Schaap, Peter J, van Passel, Mark W J, Smidt, Hauke, Sipkema, Detmer
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5765558/
https://www.ncbi.nlm.nih.gov/pubmed/29319806
http://dx.doi.org/10.1093/gbe/evx271
_version_ 1783292253971677184
author Versluis, Dennis
Nijsse, Bart
Naim, Mohd Azrul
Koehorst, Jasper J
Wiese, Jutta
Imhoff, Johannes F
Schaap, Peter J
van Passel, Mark W J
Smidt, Hauke
Sipkema, Detmer
author_facet Versluis, Dennis
Nijsse, Bart
Naim, Mohd Azrul
Koehorst, Jasper J
Wiese, Jutta
Imhoff, Johannes F
Schaap, Peter J
van Passel, Mark W J
Smidt, Hauke
Sipkema, Detmer
author_sort Versluis, Dennis
collection PubMed
description Pseudovibrio is a marine bacterial genus members of which are predominantly isolated from sessile marine animals, and particularly sponges. It has been hypothesized that Pseudovibrio spp. form mutualistic relationships with their hosts. Here, we studied Pseudovibrio phylogeny and genetic adaptations that may play a role in host colonization by comparative genomics of 31 Pseudovibrio strains, including 25 sponge isolates. All genomes were highly similar in terms of encoded core metabolic pathways, albeit with substantial differences in overall gene content. Based on gene composition, Pseudovibrio spp. clustered by geographic region, indicating geographic speciation. Furthermore, the fact that isolates from the Mediterranean Sea clustered by sponge species suggested host-specific adaptation or colonization. Genome analyses suggest that Pseudovibrio hongkongensis UST20140214-015B(T) is only distantly related to other Pseudovibrio spp., thereby challenging its status as typical Pseudovibrio member. All Pseudovibrio genomes were found to encode numerous proteins with SEL1 and tetratricopeptide repeats, which have been suggested to play a role in host colonization. For evasion of the host immune system, Pseudovibrio spp. may depend on type III, IV, and VI secretion systems that can inject effector molecules into eukaryotic cells. Furthermore, Pseudovibrio genomes carry on average seven secondary metabolite biosynthesis clusters, reinforcing the role of Pseudovibrio spp. as potential producers of novel bioactive compounds. Tropodithietic acid, bacteriocin, and terpene biosynthesis clusters were highly conserved within the genus, suggesting an essential role in survival, for example through growth inhibition of bacterial competitors. Taken together, these results support the hypothesis that Pseudovibrio spp. have mutualistic relations with sponges.
format Online
Article
Text
id pubmed-5765558
institution National Center for Biotechnology Information
language English
publishDate 2018
publisher Oxford University Press
record_format MEDLINE/PubMed
spelling pubmed-57655582018-01-16 Comparative Genomics Highlights Symbiotic Capacities and High Metabolic Flexibility of the Marine Genus Pseudovibrio Versluis, Dennis Nijsse, Bart Naim, Mohd Azrul Koehorst, Jasper J Wiese, Jutta Imhoff, Johannes F Schaap, Peter J van Passel, Mark W J Smidt, Hauke Sipkema, Detmer Genome Biol Evol Research Article Pseudovibrio is a marine bacterial genus members of which are predominantly isolated from sessile marine animals, and particularly sponges. It has been hypothesized that Pseudovibrio spp. form mutualistic relationships with their hosts. Here, we studied Pseudovibrio phylogeny and genetic adaptations that may play a role in host colonization by comparative genomics of 31 Pseudovibrio strains, including 25 sponge isolates. All genomes were highly similar in terms of encoded core metabolic pathways, albeit with substantial differences in overall gene content. Based on gene composition, Pseudovibrio spp. clustered by geographic region, indicating geographic speciation. Furthermore, the fact that isolates from the Mediterranean Sea clustered by sponge species suggested host-specific adaptation or colonization. Genome analyses suggest that Pseudovibrio hongkongensis UST20140214-015B(T) is only distantly related to other Pseudovibrio spp., thereby challenging its status as typical Pseudovibrio member. All Pseudovibrio genomes were found to encode numerous proteins with SEL1 and tetratricopeptide repeats, which have been suggested to play a role in host colonization. For evasion of the host immune system, Pseudovibrio spp. may depend on type III, IV, and VI secretion systems that can inject effector molecules into eukaryotic cells. Furthermore, Pseudovibrio genomes carry on average seven secondary metabolite biosynthesis clusters, reinforcing the role of Pseudovibrio spp. as potential producers of novel bioactive compounds. Tropodithietic acid, bacteriocin, and terpene biosynthesis clusters were highly conserved within the genus, suggesting an essential role in survival, for example through growth inhibition of bacterial competitors. Taken together, these results support the hypothesis that Pseudovibrio spp. have mutualistic relations with sponges. Oxford University Press 2018-01-08 /pmc/articles/PMC5765558/ /pubmed/29319806 http://dx.doi.org/10.1093/gbe/evx271 Text en © The Author(s) 2018. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Research Article
Versluis, Dennis
Nijsse, Bart
Naim, Mohd Azrul
Koehorst, Jasper J
Wiese, Jutta
Imhoff, Johannes F
Schaap, Peter J
van Passel, Mark W J
Smidt, Hauke
Sipkema, Detmer
Comparative Genomics Highlights Symbiotic Capacities and High Metabolic Flexibility of the Marine Genus Pseudovibrio
title Comparative Genomics Highlights Symbiotic Capacities and High Metabolic Flexibility of the Marine Genus Pseudovibrio
title_full Comparative Genomics Highlights Symbiotic Capacities and High Metabolic Flexibility of the Marine Genus Pseudovibrio
title_fullStr Comparative Genomics Highlights Symbiotic Capacities and High Metabolic Flexibility of the Marine Genus Pseudovibrio
title_full_unstemmed Comparative Genomics Highlights Symbiotic Capacities and High Metabolic Flexibility of the Marine Genus Pseudovibrio
title_short Comparative Genomics Highlights Symbiotic Capacities and High Metabolic Flexibility of the Marine Genus Pseudovibrio
title_sort comparative genomics highlights symbiotic capacities and high metabolic flexibility of the marine genus pseudovibrio
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5765558/
https://www.ncbi.nlm.nih.gov/pubmed/29319806
http://dx.doi.org/10.1093/gbe/evx271
work_keys_str_mv AT versluisdennis comparativegenomicshighlightssymbioticcapacitiesandhighmetabolicflexibilityofthemarinegenuspseudovibrio
AT nijssebart comparativegenomicshighlightssymbioticcapacitiesandhighmetabolicflexibilityofthemarinegenuspseudovibrio
AT naimmohdazrul comparativegenomicshighlightssymbioticcapacitiesandhighmetabolicflexibilityofthemarinegenuspseudovibrio
AT koehorstjasperj comparativegenomicshighlightssymbioticcapacitiesandhighmetabolicflexibilityofthemarinegenuspseudovibrio
AT wiesejutta comparativegenomicshighlightssymbioticcapacitiesandhighmetabolicflexibilityofthemarinegenuspseudovibrio
AT imhoffjohannesf comparativegenomicshighlightssymbioticcapacitiesandhighmetabolicflexibilityofthemarinegenuspseudovibrio
AT schaappeterj comparativegenomicshighlightssymbioticcapacitiesandhighmetabolicflexibilityofthemarinegenuspseudovibrio
AT vanpasselmarkwj comparativegenomicshighlightssymbioticcapacitiesandhighmetabolicflexibilityofthemarinegenuspseudovibrio
AT smidthauke comparativegenomicshighlightssymbioticcapacitiesandhighmetabolicflexibilityofthemarinegenuspseudovibrio
AT sipkemadetmer comparativegenomicshighlightssymbioticcapacitiesandhighmetabolicflexibilityofthemarinegenuspseudovibrio