Transcriptional activity of the giant barrel sponge, Xestospongia muta Holobiont: Molecular Evidence for Metabolic Interchange

Compared to our understanding of the taxonomic composition of the symbiotic microbes in marine sponges, the functional diversity of these symbionts is largely unknown. Furthermore, the application of genomic, transcriptomic, and proteomic techniques to functional questions on sponge host-symbiont in...

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Main Authors: Cara L Fiore, Micheline eLabrie, Jessica K Jarett, Michael P. Lesser
Format: Article
Language:English
Published: Frontiers Media S.A. 2015-04-01
Series:Frontiers in Microbiology
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fmicb.2015.00364/full
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spelling doaj-6237d6795ec54fe0a15f7342c66852992020-11-24T22:38:35ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2015-04-01610.3389/fmicb.2015.00364130000Transcriptional activity of the giant barrel sponge, Xestospongia muta Holobiont: Molecular Evidence for Metabolic InterchangeCara L Fiore0Micheline eLabrie1Jessica K Jarett2Michael P. Lesser3Woods Hole Oceanographic InstitutionUniversity of Massachusuettes at DartmouthUnited States Department of Energy Joint Genome InstituteUniversity of New HampshireCompared to our understanding of the taxonomic composition of the symbiotic microbes in marine sponges, the functional diversity of these symbionts is largely unknown. Furthermore, the application of genomic, transcriptomic, and proteomic techniques to functional questions on sponge host-symbiont interactions is in its infancy. In this study, we generated a transcriptome for the host and a metatranscriptome of its microbial symbionts for the giant barrel sponge, Xestospongia muta, from the Caribbean. In combination with a gene-specific approach, our goals were to 1) characterize genetic evidence for nitrogen cycling in X. muta, an important limiting nutrient on coral reefs 2) identify which prokaryotic symbiont lineages are metabolically active and, 3) characterize the metabolic potential of the prokaryotic community. Xestospongia muta expresses genes from multiple nitrogen transformation pathways that when combined with the abundance of this sponge, and previous data on dissolved inorganic nitrogen fluxes, shows that this sponge is an important contributor to nitrogen cycling on coral reefs. Additionally, we observed significant differences in gene expression of the archaeal amoA gene, which is involved in ammonia oxidation, between coral reef locations consistent with differences in the fluxes of dissolved inorganic nitrogen previously reported. In regards to symbiont metabolic potential, the genes in the biosynthetic pathways of several amino acids were present in the prokaryotic metatranscriptome dataset but in the host-derived transcripts only the catabolic reactions for these amino acids were present. A similar pattern was observed for the B vitamins (riboflavin, biotin, thiamin, cobalamin). These results expand our understanding of biogeochemical cycling in sponges, and the metabolic interchange highlighted here advances the field of symbiont physiology by elucidating specific metabolic pathways where there is high potential for host-prokaryote interactions.http://journal.frontiersin.org/Journal/10.3389/fmicb.2015.00364/fullDenitrificationammonia oxidationB vitaminsmetatranscriptomesponge symbionts
collection DOAJ
language English
format Article
sources DOAJ
author Cara L Fiore
Micheline eLabrie
Jessica K Jarett
Michael P. Lesser
spellingShingle Cara L Fiore
Micheline eLabrie
Jessica K Jarett
Michael P. Lesser
Transcriptional activity of the giant barrel sponge, Xestospongia muta Holobiont: Molecular Evidence for Metabolic Interchange
Frontiers in Microbiology
Denitrification
ammonia oxidation
B vitamins
metatranscriptome
sponge symbionts
author_facet Cara L Fiore
Micheline eLabrie
Jessica K Jarett
Michael P. Lesser
author_sort Cara L Fiore
title Transcriptional activity of the giant barrel sponge, Xestospongia muta Holobiont: Molecular Evidence for Metabolic Interchange
title_short Transcriptional activity of the giant barrel sponge, Xestospongia muta Holobiont: Molecular Evidence for Metabolic Interchange
title_full Transcriptional activity of the giant barrel sponge, Xestospongia muta Holobiont: Molecular Evidence for Metabolic Interchange
title_fullStr Transcriptional activity of the giant barrel sponge, Xestospongia muta Holobiont: Molecular Evidence for Metabolic Interchange
title_full_unstemmed Transcriptional activity of the giant barrel sponge, Xestospongia muta Holobiont: Molecular Evidence for Metabolic Interchange
title_sort transcriptional activity of the giant barrel sponge, xestospongia muta holobiont: molecular evidence for metabolic interchange
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2015-04-01
description Compared to our understanding of the taxonomic composition of the symbiotic microbes in marine sponges, the functional diversity of these symbionts is largely unknown. Furthermore, the application of genomic, transcriptomic, and proteomic techniques to functional questions on sponge host-symbiont interactions is in its infancy. In this study, we generated a transcriptome for the host and a metatranscriptome of its microbial symbionts for the giant barrel sponge, Xestospongia muta, from the Caribbean. In combination with a gene-specific approach, our goals were to 1) characterize genetic evidence for nitrogen cycling in X. muta, an important limiting nutrient on coral reefs 2) identify which prokaryotic symbiont lineages are metabolically active and, 3) characterize the metabolic potential of the prokaryotic community. Xestospongia muta expresses genes from multiple nitrogen transformation pathways that when combined with the abundance of this sponge, and previous data on dissolved inorganic nitrogen fluxes, shows that this sponge is an important contributor to nitrogen cycling on coral reefs. Additionally, we observed significant differences in gene expression of the archaeal amoA gene, which is involved in ammonia oxidation, between coral reef locations consistent with differences in the fluxes of dissolved inorganic nitrogen previously reported. In regards to symbiont metabolic potential, the genes in the biosynthetic pathways of several amino acids were present in the prokaryotic metatranscriptome dataset but in the host-derived transcripts only the catabolic reactions for these amino acids were present. A similar pattern was observed for the B vitamins (riboflavin, biotin, thiamin, cobalamin). These results expand our understanding of biogeochemical cycling in sponges, and the metabolic interchange highlighted here advances the field of symbiont physiology by elucidating specific metabolic pathways where there is high potential for host-prokaryote interactions.
topic Denitrification
ammonia oxidation
B vitamins
metatranscriptome
sponge symbionts
url http://journal.frontiersin.org/Journal/10.3389/fmicb.2015.00364/full
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