Metaphylogenomic and Potential Functionality of the Limpet Patella pellucida’s Gastrointestinal Tract Microbiome

Dudek, Magda; Adams, Jessica; Swain, Martin; Hegarty, Matthew J.; Huws, Sharon; Gallagher, Joe

doi:10.3390/ijms151018819

Cited by 15 publications

(19 citation statements)

References 102 publications

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“…Proteobacteria, for example, is the most abundant phylum present in each gastropod species, as well as in the environmental controls. This is consistent with previous studies that have shown members of this phylum to dominate host‐associated microbiota in marine animals including limpets, corals, copepods and fish (Bayer et al ., ; Dudek et al ., ; Givens et al ., ; Dorosz et al ., ). However, preferential enrichment of different genera, such as Mycoplasma in C. funebralis and Psychrilyobacter in L. gigantea, contributes to significant differences among microbiomes of our four gastropod hosts.…”

Section: Discussionmentioning

confidence: 98%

“…Marine molluscs are one of the most diverse and ecologically important groups of marine invertebrates, with many species providing a variety of ecosystem services including supporting commercial and artisanal fisheries. Information about the diversity and compositions of microbes associated with molluscan hosts still remains scarce, although microbiomes of some bivalve (Prieur et al, 1990;Betcher et al, 2012;King et al, 2012;Lokmer et al, 2016;Pierce et al, 2016;Arfken et al, 2017) and gastropod (Dudek et al, 2014;Zbinden et al, 2014;Aronson et al, 2017;Cicala et al, 2018) species have been quantified. Moreover, existing analyses of marine gastropod microbiomes have primarily focused on the digestive tract, with only one study including gillspecific microbiome data (Zbinden et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

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Diversity and composition of intertidal gastropod microbiomes across a major marine biogeographic boundary

Neu

Allen

Roy

2019

Environ Microbiol Rep

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Summary Marine biogeographic boundaries act as barriers to dispersal for many animal species, thereby creating distinctive faunas on either side. However, how such boundaries affect the distributions of microbial taxa remains poorly known. To test whether biogeographic boundaries influence the diversity and composition of host‐associated microbiota, we analysed the microbiomes of three species of common intertidal gastropods at two sites separated by the biogeographic boundary at Point Conception (PtC), CA, using 16S rRNA gene sequencing. Our results show that each host species shows microbiome compositional specificity, even across PtC, and that alpha diversity does not change significantly across this boundary for any of the gastropod hosts. However, for two of the host species, beta diversity differs significantly across PtC, indicating that there may be multiple levels of organization of the marine gastropod microbiome. Overall, our results suggest that while biogeographic boundaries do not constrain the distribution of a core set of microbes associated with each host species, they can play a role in structuring the transient portion of the microbiome.

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Section: Discussionmentioning

confidence: 98%

Section: Introductionmentioning

confidence: 99%

Diversity and composition of intertidal gastropod microbiomes across a major marine biogeographic boundary

Neu

Allen

Roy

2019

Environ Microbiol Rep

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“…Indeed, anaerobic bacteria from the classes Fusobacteriia and Mollicutes are only rarely found in coastal waters or associated with macroalgae [ 39 – 41 ]. However, these bacterial groups seem rather typical of digestive organs of marine holobionts as they are found in the sea squirt Ciona intestinalis , the limpet Patella pellucida , and marine carnivores [ 21 , 42 , 43 ]. Members of Vibrio are well known as pathogen of animals, and it is the most common bacterial genus in guts of marine animals such as the intestinal mucosa of marine fishes [ 35 , 44 – 46 ].…”

Section: Discussionmentioning

confidence: 99%

“…Most marine herbivores are generalists, meaning they are able to feed on the three macroalgal lineages, but only few studies have been performed on digestive microbiota in marine herbivores. Bacteria have been shown to help degrade macroalgal polysaccharides in the sea hare Aplysia spp., the snail Tegula funebralis , the limpet Patella pellucida , and the iguana Amblyrhynchus cristatus [ 21 – 24 ], but these studies considered neither different diet types nor seasonality. The abalone, a gastropod of high economic interest especially in China, Korea, South Africa, and Chile [ 25 , 26 ], is also a generalist herbivore [ 27 ], but its digestive enzymes are not sufficient for macroalgal polysaccharide degradation [ 28 ].…”

Section: Introductionmentioning

confidence: 99%

Seasonal and algal diet-driven patterns of the digestive microbiota of the European abalone Haliotis tuberculata, a generalist marine herbivore

et al. 2018

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BackgroundHolobionts have a digestive microbiota with catabolic abilities allowing the degradation of complex dietary compounds for the host. In terrestrial herbivores, the digestive microbiota is known to degrade complex polysaccharides from land plants while in marine herbivores, the digestive microbiota is poorly characterized. Most of the latter are generalists and consume red, green, and brown macroalgae, three distinct lineages characterized by a specific composition in complex polysaccharides, which represent half of their biomass. Subsequently, each macroalga features a specific epiphytic microbiota, and the digestive microbiota of marine herbivores is expected to vary with a monospecific algal diet. We investigated the effect of four monospecific diets (Palmaria palmata, Ulva lactuca, Saccharina latissima, Laminaria digitata) on the composition and specificity of the digestive microbiota of a generalist marine herbivore, the abalone, farmed in a temperate coastal area over a year. The microbiota from the abalone digestive gland was sampled every 2 months and explored using metabarcoding.ResultsDiversity and multivariate analyses showed that patterns of the microbiota were significantly linked to seasonal variations of contextual parameters but not directly to a specific algal diet. Three core genera: Psychrilyobacter, Mycoplasma, and Vibrio constantly dominated the microbiota in the abalone digestive gland. Additionally, a less abundant and diet-specific core microbiota featured genera representing aerobic primary degraders of algal polysaccharides.ConclusionsThis study highlights the establishment of a persistent core microbiota in the digestive gland of the abalone since its juvenile state and the presence of a less abundant and diet-specific core community. While composed of different microbial taxa compared to terrestrial herbivores, the digestive gland constitutes a particular niche in the abalone holobiont, where bacteria (i) may cooperate to degrade algal polysaccharides to products assimilable by the host or (ii) may have acquired these functions through gene transfer from the aerobic algal microbiota.Electronic supplementary materialThe online version of this article (10.1186/s40168-018-0430-7) contains supplementary material, which is available to authorized users.

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“…Another metagenomic study of the 16S rRNA gene of a bivalve mollusc (internal body parts without the shell) resulted in the discovery of 3553 OTUs from 44 phyla, in which Proteobacteria was found to be the most abundant phylum [ 52 ]. The metagenome of the digestive tract of a marine limpet also revealed diverse microbial communities with the most dominant phylum being Proteobacteria [ 53 ]. Indeed, Proteobacteria accounts for more than 40% of all known prokaryotic genera [ 54 ] and is the dominant bacterial phyla reported from other marine invertebrate taxa, including the sponge Halichondria sp.…”

Section: Discussionmentioning

confidence: 99%

Characterization of Bacterial Communities Associated with the Tyrian Purple Producing Gland in a Marine Gastropod

et al. 2015

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Dicathais orbita is a marine mollusc recognised for the production of anticancer compounds that are precursors to Tyrian purple. This study aimed to assess the diversity and identity of bacteria associated with the Tyrian purple producing hypobranchial gland, in comparison with foot tissue, using a high-throughput sequencing approach. Taxonomic and phylogenetic analysis of variable region V1-V3 of 16S rRNA bacterial gene amplicons in QIIME and MEGAN were carried out. This analysis revealed a highly diverse bacterial assemblage associated with the hypobranchial gland and foot tissues of D. orbita. The dominant bacterial phylum in the 16S rRNA bacterial profiling data set was Proteobacteria followed by Bacteroidetes, Tenericutes and Spirochaetes. In comparison to the foot, the hypobranchial gland had significantly lower bacterial diversity and a different community composition, based on taxonomic assignment at the genus level. A higher abundance of indole producing Vibrio spp. and the presence of bacteria with brominating capabilities in the hypobranchial gland suggest bacteria have a potential role in biosynthesis of Tyrian purple in D. orbita.

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Metaphylogenomic and Potential Functionality of the Limpet Patella pellucida’s Gastrointestinal Tract Microbiome

Cited by 15 publications

References 102 publications

Diversity and composition of intertidal gastropod microbiomes across a major marine biogeographic boundary

Diversity and composition of intertidal gastropod microbiomes across a major marine biogeographic boundary

Seasonal and algal diet-driven patterns of the digestive microbiota of the European abalone Haliotis tuberculata, a generalist marine herbivore

Characterization of Bacterial Communities Associated with the Tyrian Purple Producing Gland in a Marine Gastropod

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