Phylogenetic Diversity, Distribution, and Cophylogeny of Giant Bacteria (Epulopiscium) with their Surgeonfish Hosts in the Red Sea

Handle URI:
http://hdl.handle.net/10754/608627
Title:
Phylogenetic Diversity, Distribution, and Cophylogeny of Giant Bacteria (Epulopiscium) with their Surgeonfish Hosts in the Red Sea
Authors:
Miyake, Sou ( 0000-0001-7507-1653 ) ; Ngugi, David ( 0000-0002-0442-4279 ) ; Stingl, Ulrich ( 0000-0002-0684-2597 )
Abstract:
Epulopiscium is a group of giant bacteria found in high abundance in intestinal tracts of herbivorous surgeonfish. Despite their peculiarly large cell size (can be up to 600 μm), extreme polyploidy (some with over 100,000 genome copies per cell) and viviparity (whereby mother cells produce live offspring), details about their diversity, distribution or their role in the host gut are lacking. Previous studies have highlighted the existence of morphologically distinct Epulopiscium cell types (defined as morphotypes A to J) in some surgeonfish genera, but the corresponding genetic diversity and distribution among other surgeonfishes remain mostly unknown. Therefore, we investigated the phylogenetic diversity of Epulopiscium, distribution and co-occurrence in multiple hosts. Here, we identified eleven new phylogenetic clades, six of which were also morphologically characterized. Three of these novel clades were phylogenetically and morphologically similar to cigar-shaped type A1 cells, found in a wide range of surgeonfishes including Acanthurus nigrofuscus, while three were similar to smaller, rod-shaped type E that has not been phylogenetically classified thus far. Our results also confirmed that biogeography appears to have relatively little influence on Epulopiscium diversity, as clades found in the Great Barrier Reef and Hawaii were also recovered from the Red Sea. Although multiple symbiont clades inhabited a given species of host surgeonfish and multiple host species possessed a given symbiont clade, statistical analysis of host and symbiont phylogenies indicated significant cophylogeny, which in turn suggests co-evolutionary relationships. A cluster analysis of Epulopiscium sequences from previously published amplicon sequencing dataset revealed a similar pattern, where specific clades were consistently found in high abundance amongst closely related surgeonfishes. Differences in abundance may indicate specialization of clades to certain gut environments reflected by inferred differences in the host diets. Overall, our analysis identified a large phylogenetic diversity of Epulopiscium (up to 10% sequence divergence of 16S rRNA genes), which lets us hypothesize that there are multiple species that are spread across guts of different host species.
KAUST Department:
Marine Microbial Ecology Research Group; Red Sea Research Center (RSRC)
Citation:
Phylogenetic Diversity, Distribution, and Cophylogeny of Giant Bacteria (Epulopiscium) with their Surgeonfish Hosts in the Red Sea 2016, 7 Frontiers in Microbiology
Publisher:
Frontiers Media SA
Journal:
Frontiers in Microbiology
Issue Date:
14-Mar-2016
DOI:
10.3389/fmicb.2016.00285
Type:
Article
ISSN:
1664-302X
Sponsors:
The research reported here was supported by King Abdullah University of Science and Technology (KAUST). We would like to thank Dr. John Howard Choat and Dr. William D. Robbins (James Cook University, Australia) for providing us with the host fish diet information and discussions related to the host diet. We also thank Dr. Matthew Cahill on his invaluable input and expertise, and Professor Michael L. Berumen, Dr. Joseph DiBattista, and Tane H. Sinclair-Taylor for assistance with fish sampling. We also extend our thanks to the KAUST Coastal and Marine Resources Core Lab and the Bioscience Core Lab for their technical assistance.
Additional Links:
http://journal.frontiersin.org/Article/10.3389/fmicb.2016.00285/abstract
Appears in Collections:
Articles; Red Sea Research Center (RSRC)

Full metadata record

DC FieldValue Language
dc.contributor.authorMiyake, Souen
dc.contributor.authorNgugi, Daviden
dc.contributor.authorStingl, Ulrichen
dc.date.accessioned2016-05-09T08:19:05Zen
dc.date.available2016-05-09T08:19:05Zen
dc.date.issued2016-03-14en
dc.identifier.citationPhylogenetic Diversity, Distribution, and Cophylogeny of Giant Bacteria (Epulopiscium) with their Surgeonfish Hosts in the Red Sea 2016, 7 Frontiers in Microbiologyen
dc.identifier.issn1664-302Xen
dc.identifier.doi10.3389/fmicb.2016.00285en
dc.identifier.urihttp://hdl.handle.net/10754/608627en
dc.description.abstractEpulopiscium is a group of giant bacteria found in high abundance in intestinal tracts of herbivorous surgeonfish. Despite their peculiarly large cell size (can be up to 600 μm), extreme polyploidy (some with over 100,000 genome copies per cell) and viviparity (whereby mother cells produce live offspring), details about their diversity, distribution or their role in the host gut are lacking. Previous studies have highlighted the existence of morphologically distinct Epulopiscium cell types (defined as morphotypes A to J) in some surgeonfish genera, but the corresponding genetic diversity and distribution among other surgeonfishes remain mostly unknown. Therefore, we investigated the phylogenetic diversity of Epulopiscium, distribution and co-occurrence in multiple hosts. Here, we identified eleven new phylogenetic clades, six of which were also morphologically characterized. Three of these novel clades were phylogenetically and morphologically similar to cigar-shaped type A1 cells, found in a wide range of surgeonfishes including Acanthurus nigrofuscus, while three were similar to smaller, rod-shaped type E that has not been phylogenetically classified thus far. Our results also confirmed that biogeography appears to have relatively little influence on Epulopiscium diversity, as clades found in the Great Barrier Reef and Hawaii were also recovered from the Red Sea. Although multiple symbiont clades inhabited a given species of host surgeonfish and multiple host species possessed a given symbiont clade, statistical analysis of host and symbiont phylogenies indicated significant cophylogeny, which in turn suggests co-evolutionary relationships. A cluster analysis of Epulopiscium sequences from previously published amplicon sequencing dataset revealed a similar pattern, where specific clades were consistently found in high abundance amongst closely related surgeonfishes. Differences in abundance may indicate specialization of clades to certain gut environments reflected by inferred differences in the host diets. Overall, our analysis identified a large phylogenetic diversity of Epulopiscium (up to 10% sequence divergence of 16S rRNA genes), which lets us hypothesize that there are multiple species that are spread across guts of different host species.en
dc.description.sponsorshipThe research reported here was supported by King Abdullah University of Science and Technology (KAUST). We would like to thank Dr. John Howard Choat and Dr. William D. Robbins (James Cook University, Australia) for providing us with the host fish diet information and discussions related to the host diet. We also thank Dr. Matthew Cahill on his invaluable input and expertise, and Professor Michael L. Berumen, Dr. Joseph DiBattista, and Tane H. Sinclair-Taylor for assistance with fish sampling. We also extend our thanks to the KAUST Coastal and Marine Resources Core Lab and the Bioscience Core Lab for their technical assistance.en
dc.language.isoenen
dc.publisherFrontiers Media SAen
dc.relation.urlhttp://journal.frontiersin.org/Article/10.3389/fmicb.2016.00285/abstracten
dc.rightsThis is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.en
dc.subjectEpulopisciumen
dc.subjectcoevolutionen
dc.subjectsurgeonfishen
dc.subjectRed Seaen
dc.subject16S rRNAen
dc.titlePhylogenetic Diversity, Distribution, and Cophylogeny of Giant Bacteria (Epulopiscium) with their Surgeonfish Hosts in the Red Seaen
dc.typeArticleen
dc.contributor.departmentMarine Microbial Ecology Research Groupen
dc.contributor.departmentRed Sea Research Center (RSRC)en
dc.identifier.journalFrontiers in Microbiologyen
dc.eprint.versionPublisher's Version/PDFen
dc.contributor.affiliationKing Abdullah University of Science and Technology (KAUST)en
kaust.authorMiyake, Souen
kaust.authorNgugi, Daviden
kaust.authorStingl, Ulrichen
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