A Simple Microbiome in the European Common Cuttlefish, Sepia officinalis

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.

In Vivo Mercury (De)Methylation Metabolism in Cephalopods under Different pCO2 Scenarios

“…The analysis of the gut microbiota diversity in cuttlefish revealed a very simple microbiome, with Mycoplasma sp. being the most abundant genus of bacteria, as observed by Lutz et al and Ramírez et al To our knowledge, it is the first study highlighting the presence of a microbiome associated with the digestive gland of cuttlefish. This microbiome is diverse when compared to the gut microbiome.…”

Ecology and Host Identity Outweigh Evolutionary History in Shaping the Bat Microbiome

“…We did not find a significant correlation between host phylogenetic distance and microbial dissimilarity, suggesting that any pattern of phylosymbiosis observed in bats is not driven by host evolution, but rather by ecological features. Investigation of microbial loads via culturebased approaches and quantitative PCR (qPCR) paired with observed spatial arrangements (e.g., via fluorescence in situ hybridization [68,69]) throughout the gut and other anatomical sites of bats will provide important insights into the nature of bat-microbe associations and whether they are sustained, functional associations or transient en-counters between bats and their environments. Analysis of morphological and physiological adaptations specific to flight in bats may also help elucidate why bats differ from nonflighted mammals with respect to the weak pattern of phylosymbiosis observed in this study.…”

Microbial community characteristics of the intestine and gills of medium-form populations of Sthenoteuthis oualaniensis in the South China Sea

“…Strugnell and Nishiguchi (2007) analyzed the cephalopod intestinal microbial community in freeliving and captive Octopus minor paralarvae using nextgeneration sequencing. A recent study confirmed the microbial composition of the digestive tract, gills, and skin microbiome of Sepia officinalis (Lutz et al, 2019). The populations of S. oualaniensis are one of the most promising biological resources in the South China Sea because of their short life cycles (Zhang et al, 2010).…”