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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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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