A Simple Microbiome in the European Common Cuttlefish, <italic toggle="yes">Sepia officinalis</italic>

ABSTRACT The European common cuttlefish, Sepia officinalis, is used extensively in biological and biomedical research, yet its microbiome remains poorly characterized. We analyzed the microbiota of the digestive tract, gills, and skin in mariculture-raised S. officinalis using a combination of 16S r...

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Autores principales:	Holly L. Lutz, S. Tabita Ramírez-Puebla, Lisa Abbo, Amber Durand, Cathleen Schlundt, Neil R. Gottel, Alexandra K. Sjaarda, Roger T. Hanlon, Jack A. Gilbert, Jessica L. Mark Welch
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Cephalopoda Piscirickettsiaceae Vibrionaceae enrofloxacin fluorescence assays microbiome Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/7fb540df042043e080b0920ab0d5ed1b
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spelling	oai:doaj.org-article:7fb540df042043e080b0920ab0d5ed1b2021-12-02T18:25:16ZA Simple Microbiome in the European Common Cuttlefish, <italic toggle="yes">Sepia officinalis</italic>10.1128/mSystems.00177-192379-5077https://doaj.org/article/7fb540df042043e080b0920ab0d5ed1b2019-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00177-19https://doaj.org/toc/2379-5077ABSTRACT The European common cuttlefish, Sepia officinalis, is used extensively in biological and biomedical research, yet its microbiome remains poorly characterized. We analyzed the microbiota of the digestive tract, gills, and skin in mariculture-raised S. officinalis using a combination of 16S rRNA amplicon sequencing, quantitative PCR (qPCR), and fluorescence spectral imaging. Sequencing revealed a highly simplified microbiota consisting largely of two single bacterial amplicon sequence variants (ASVs) of Vibrionaceae and Piscirickettsiaceae. The esophagus was dominated by a single ASV of the genus Vibrio. Imaging revealed bacteria in the family Vibrionaceae distributed in a discrete layer that lines the esophagus. This Vibrio was also the primary ASV found in the microbiota of the stomach, cecum, and intestine, but occurred at lower abundance, as determined by qPCR, and was found only scattered in the lumen rather than in a discrete layer via imaging analysis. Treatment of animals with the commonly used antibiotic enrofloxacin led to a nearly 80% reduction of the dominant Vibrio ASV in the esophagus but did not significantly alter the relative abundance of bacteria overall between treated versus control animals. Data from the gills were dominated by a single ASV in the family Piscirickettsiaceae, which imaging visualized as small clusters of cells. We conclude that bacteria belonging to the Gammaproteobacteria are the major symbionts of the cuttlefish Sepia officinalis cultured from eggs in captivity and that the esophagus and gills are major colonization sites. IMPORTANCE Microbes can play critical roles in the physiology of their animal hosts, as evidenced in cephalopods by the role of Vibrio (Aliivibrio) fischeri in the light organ of the bobtail squid and the role of Alpha- and Gammaproteobacteria in the reproductive system and egg defense in a variety of cephalopods. We sampled the cuttlefish microbiome throughout the digestive tract, gills, and skin and found dense colonization of an unexpected site, the esophagus, by a microbe of the genus Vibrio, as well as colonization of gills by Piscirickettsiaceae. This finding expands the range of organisms and body sites known to be associated with Vibrio and is of potential significance for understanding host-symbiont associations, as well as for understanding and maintaining the health of cephalopods in mariculture.Holly L. LutzS. Tabita Ramírez-PueblaLisa AbboAmber DurandCathleen SchlundtNeil R. GottelAlexandra K. SjaardaRoger T. HanlonJack A. GilbertJessica L. Mark WelchAmerican Society for MicrobiologyarticleCephalopodaPiscirickettsiaceaeVibrionaceaeenrofloxacinfluorescence assaysmicrobiomeMicrobiologyQR1-502ENmSystems, Vol 4, Iss 4 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Cephalopoda Piscirickettsiaceae Vibrionaceae enrofloxacin fluorescence assays microbiome Microbiology QR1-502
spellingShingle	Cephalopoda Piscirickettsiaceae Vibrionaceae enrofloxacin fluorescence assays microbiome Microbiology QR1-502 Holly L. Lutz S. Tabita Ramírez-Puebla Lisa Abbo Amber Durand Cathleen Schlundt Neil R. Gottel Alexandra K. Sjaarda Roger T. Hanlon Jack A. Gilbert Jessica L. Mark Welch A Simple Microbiome in the European Common Cuttlefish, <italic toggle="yes">Sepia officinalis</italic>
description	ABSTRACT The European common cuttlefish, Sepia officinalis, is used extensively in biological and biomedical research, yet its microbiome remains poorly characterized. We analyzed the microbiota of the digestive tract, gills, and skin in mariculture-raised S. officinalis using a combination of 16S rRNA amplicon sequencing, quantitative PCR (qPCR), and fluorescence spectral imaging. Sequencing revealed a highly simplified microbiota consisting largely of two single bacterial amplicon sequence variants (ASVs) of Vibrionaceae and Piscirickettsiaceae. The esophagus was dominated by a single ASV of the genus Vibrio. Imaging revealed bacteria in the family Vibrionaceae distributed in a discrete layer that lines the esophagus. This Vibrio was also the primary ASV found in the microbiota of the stomach, cecum, and intestine, but occurred at lower abundance, as determined by qPCR, and was found only scattered in the lumen rather than in a discrete layer via imaging analysis. Treatment of animals with the commonly used antibiotic enrofloxacin led to a nearly 80% reduction of the dominant Vibrio ASV in the esophagus but did not significantly alter the relative abundance of bacteria overall between treated versus control animals. Data from the gills were dominated by a single ASV in the family Piscirickettsiaceae, which imaging visualized as small clusters of cells. We conclude that bacteria belonging to the Gammaproteobacteria are the major symbionts of the cuttlefish Sepia officinalis cultured from eggs in captivity and that the esophagus and gills are major colonization sites. IMPORTANCE Microbes can play critical roles in the physiology of their animal hosts, as evidenced in cephalopods by the role of Vibrio (Aliivibrio) fischeri in the light organ of the bobtail squid and the role of Alpha- and Gammaproteobacteria in the reproductive system and egg defense in a variety of cephalopods. We sampled the cuttlefish microbiome throughout the digestive tract, gills, and skin and found dense colonization of an unexpected site, the esophagus, by a microbe of the genus Vibrio, as well as colonization of gills by Piscirickettsiaceae. This finding expands the range of organisms and body sites known to be associated with Vibrio and is of potential significance for understanding host-symbiont associations, as well as for understanding and maintaining the health of cephalopods in mariculture.
format	article
author	Holly L. Lutz S. Tabita Ramírez-Puebla Lisa Abbo Amber Durand Cathleen Schlundt Neil R. Gottel Alexandra K. Sjaarda Roger T. Hanlon Jack A. Gilbert Jessica L. Mark Welch
author_facet	Holly L. Lutz S. Tabita Ramírez-Puebla Lisa Abbo Amber Durand Cathleen Schlundt Neil R. Gottel Alexandra K. Sjaarda Roger T. Hanlon Jack A. Gilbert Jessica L. Mark Welch
author_sort	Holly L. Lutz
title	A Simple Microbiome in the European Common Cuttlefish, <italic toggle="yes">Sepia officinalis</italic>
title_short	A Simple Microbiome in the European Common Cuttlefish, <italic toggle="yes">Sepia officinalis</italic>
title_full	A Simple Microbiome in the European Common Cuttlefish, <italic toggle="yes">Sepia officinalis</italic>
title_fullStr	A Simple Microbiome in the European Common Cuttlefish, <italic toggle="yes">Sepia officinalis</italic>
title_full_unstemmed	A Simple Microbiome in the European Common Cuttlefish, <italic toggle="yes">Sepia officinalis</italic>
title_sort	simple microbiome in the european common cuttlefish, <italic toggle="yes">sepia officinalis</italic>
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/7fb540df042043e080b0920ab0d5ed1b
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A Simple Microbiome in the European Common Cuttlefish, <italic toggle="yes">Sepia officinalis</italic>

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