Taxonomic and functional heterogeneity of the gill microbiome in a symbiotic coastal mangrove lucinid species

Lim, Shen Jean; Davis, Brenton G.; Gill, Danielle Elise; Walton, Jillian; Nachman, Erika; Engel, Annette Summers; Anderson, Laurie C.; Campbell, Barbara J.

doi:10.1038/s41396-018-0318-3

Cited by 49 publications

(73 citation statements)

References 118 publications

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“…We searched for these symbiont-related sequences in the uncultured Gammaproteobacteria sequences from our NGS analysis, but we unable to identify them. Since some bivalves acquire their symbionts from the environments in which they live like sediments (Gros et al, 2012;Lim et al, 2019), while abalones inhabit on reefs, we assumed that sulfur-oxidized Gammaproteobacteria was not detected in all samples.…”

Section: Discussionmentioning

confidence: 99%

Microbial community analysis in the gills of abalones suggested possible dominance of epsilonproteobacterium in Haliotis gigantea

Mizutani

Mori

Miyazaki

et al. 2020

PeerJ

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Gills are important organs for aquatic invertebrates because they harbor chemosynthetic bacteria, which fix inorganic carbon and/or nitrogen and provide their hosts with organic compounds. Nevertheless, in contrast to the intensive researches related to the gut microbiota, much is still needed to further understand the microbiota within the gills of invertebrates. Using abalones as a model, we investigated the community structure of microbes associated with the gills of these invertebrates using next-generation sequencing. Molecular identification of representative bacterial sequences was performed using cloning, nested PCR and fluorescence in situ hybridization (FISH) analysis with specific primers or probes. We examined three abalone species, namely Haliotis gigantea, H. discus and H. diversicolor using seawater and stones as controls. Microbiome analysis suggested that the gills of all three abalones had the unclassified Spirochaetaceae (one OTU, 15.7 ± 0.04%) and Mycoplasma sp. (one OTU, 9.1 ± 0.03%) as the core microbes. In most libraries from the gills of H. gigantea, however, a previously unknown epsilonproteobacterium species (one OTU) was considered as the dominant bacterium, which accounted for 62.2% of the relative abundance. The epsilonproteobacterium was only detected in the gills of H. diversicolor at 0.2% and not in H. discus suggesting that it may be unique to H. gigantea. Phylogenetic analysis performed using a near full-length 16S rRNA gene placed the uncultured epsilonproteobacterium species at the root of the family Helicobacteraceae. Interestingly, the uncultured epsilonproteobacterium was commonly detected from gill tissue rather than from the gut and foot tissues using a nested PCR assay with uncultured epsilonproteobacterium-specific primers. FISH analysis with the uncultured epsilonproteobacterium-specific probe revealed that probe-reactive cells in H. gigantea had a coccus-like morphology and formed microcolonies on gill tissue. This is the first report to show that epsilonproteobacterium has the potential to be a dominant species in the gills of the coastal gastropod, H. gigantea.

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Section: Discussionmentioning

confidence: 99%

Microbial community analysis in the gills of abalones suggested possible dominance of epsilonproteobacterium in Haliotis gigantea

Mizutani

Mori

Miyazaki

et al. 2020

PeerJ

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“…All extant lucinid species examined to date host chemosynthetic bacterial endosymbionts belonging to the class Gammaproteobacteria within specialized epithelial gill cells known as bacteriocytes (3). Lucinid gill endosymbionts possess a diverse and varied suite of functions, including thioautotrophy (4), aerobic respiration (5), assimilatory and dissimilatory nitrate reduction (6), mixotrophy (7, 8), hydrogenotrophy (7, 8), and diazotrophy (7, 9), which enable lucinids to colonize otherwise uninhabitable conditions (10). Specifically, lucinids burrow into sediments where oxygen is available from the oxic water column and dissolved sulfide is present due to the decomposition of organic matter via sulfate reduction (2, 3, 11).…”

Section: Introductionmentioning

confidence: 99%

“…Based on their 16S rRNA gene sequences, lucinid endosymbionts occur in three distinct clades, with the largest (clade A) originating from hosts that primarily inhabit sediments from seagrass beds and two (clades B and C) originating from lucinids that are more likely to inhabit sediments from mangrove-rich areas (20). It is possible that each clade represents a separate species (8), although an insufficient number of lucinid species has been examined at a sufficiently high genetic resolution to test this hypothesis. At present, low to no variability among clade A lucinid endosymbiont 16S rRNA gene sequences suggests that this group belongs to a single species (20–23).…”

Section: Introductionmentioning

confidence: 99%

“…To date, endosymbiont functions for two clade A endosymbionts, “ Candidatus Thiodiazotropha endolucinida” from Codakia orbicularis (9) and “ Ca. Thiodiazotropha endoloripes” from Loripes orbiculatus (syn = Loripes lucinalis) (7), as well as for the clade C endosymbiont from mangrove-dwelling Phacoides pectinatus (8), have been investigated using omics approaches. However, limited attention was given to species- and strain-level diversity among the endosymbiont populations.…”

Section: Introductionmentioning

confidence: 99%

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Extensive Thioautotrophic Gill Endosymbiont Diversity within a Single Ctena orbiculata (Bivalvia: Lucinidae) Population and Implications for Defining Host-Symbiont Specificity and Species Recognition

et al. 2019

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Seagrass-dwelling members of the bivalve family Lucinidae harbor environmentally acquired gill endosymbionts. According to previous studies, lucinid symbionts potentially represent multiple strains from a single thioautotrophic gammaproteobacterium species. This study utilized genomic- and transcriptomic-level data to resolve symbiont taxonomic, genetic, and functional diversity from Ctena orbiculata endosymbiont populations inhabiting carbonate-rich sediment at Sugarloaf Key, FL (USA). The sediment had mixed seagrass and calcareous green alga coverage and also was colonized by at least five other lucinid species. Four coexisting, thioautotrophic endosymbiont operational taxonomic units (OTUs), likely representing four strains from two different bacterial species, were identified from C. orbiculata. Three of these OTUs also occurred at high relative abundances in the other sympatric lucinid species. Interspecies genetic differences averaged about 5% lower at both pairwise average nucleotide identity and amino acid identity than interstrain differences. Despite these genetic differences, C. orbiculata endosymbionts shared a high number of metabolic functions, including highly expressed thioautotrophy-related genes and a moderately to weakly expressed conserved one-carbon (C1) oxidation gene cluster previously undescribed in lucinid symbionts. Few symbiont- and host-related genes, including those encoding symbiotic sulfurtransferase, host respiratory functions, and host sulfide oxidation functions, were differentially expressed between seagrass- and alga-covered sediment locations. In contrast to previous studies, the identification of multiple endosymbiont taxa within and across C. orbiculata individuals, which were also shared with other sympatric lucinid species, suggests that neither host nor endosymbiont displays strict taxonomic specificity. This necessitates further investigations into the nature and extent of specificity of lucinid hosts and their symbionts. IMPORTANCE Symbiont diversity and host/symbiont functions have been comprehensively profiled for only a few lucinid species. In this work, unprecedented thioautotrophic gill endosymbiont taxonomic diversity was characterized within a Ctena orbiculata population associated with both seagrass- and alga-covered sediments. Endosymbiont metabolisms included known chemosynthetic functions and an additional conserved, previously uncharacterized C1 oxidation pathway. Lucinid-symbiont associations were not species specific because this C. orbiculata population hosted multiple endosymbiont strains and species, and other sympatric lucinid species shared overlapping symbiont 16S rRNA gene diversity profiles with C. orbiculata. Our results suggest that lucinid-symbiont association patterns within some host species could be more taxonomically diverse than previously thought. As such, this study highlights the importance of holistic analyses, at the population, community, and even ecosystem levels, in understanding host-microbe association patterns.

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“…Manuscript to be reviewed in which they live like sediments (Gros et al 2012 andLim et al 2019), while abalones inhabit on reefs, we assumed that sulfur-oxidized Gammaproteobacteria was not detected in all samples.…”

Section: Discussionmentioning

confidence: 99%

Peer Review #1 of "Microbial community analysis in the gills of abalones suggested possible dominance of epsilonproteobacterium in Haliotis gigantea (v0.1)"

Sawabe¹

2020

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Gills are important organs for aquatic invertebrates because they harbor chemosynthetic bacteria, which fix inorganic carbon and/or nitrogen and provide their hosts with organic compounds. Nevertheless, in contrast to the intensive researches related to the gut microbiota, much is still needed to further understand the microbiota within the gills of invertebrates. Using abalones as a model, we investigated the community structure of microbes associated with the gills of these invertebrates using next-generation sequencing. Molecular identification of representative bacterial sequences was performed using cloning, nested PCR, and fluorescence in situ hybridization (FISH) analysis with specific primers or probes. We examined three abalone species, namely Haliotis gigantea, H. discus and H. diversicolor using seawater and stones as controls. Microbiome analysis suggested that the gills of all three abalones had the unclassified Spirochaetaceae (1 OTU, 15.7±0.04%) and Mycoplasma sp. (1 OTU, 9.1±0.03%) as the core microbes. In most libraries from the gills of H. gigantea, however, a previously unknown epsilonproteobacterium species (1 OTU) was considered as the dominant bacterium, which accounted for 62.2% of the relative abundance. The epsilonproteobacterium was only detected in the gills of H. diversicolor at 0.2% and not in H. discus suggesting that it may be unique to H. gigantea. Phylogenetic analysis performed using a near full-length 16S rRNA gene placed the uncultured epsilonproteobacterium species at the root of the family Helicobacteraceae. Interestingly, the uncultured epsilonproteobacterium was commonly detected from gill tissue rather than from the gut and foot tissues using a nested PCR assay with uncultured epsilonproteobacterium-specific primers. FISH analysis with the uncultured epsilonproteobacterium-specific probe revealed that probe-reactive cells in H. gigantea had a coccus-like morphology and formed microcolonies on gill tissue. This is the first report to show that epsilonproteobacterium has the potential to be a dominant species in the gills of the coastal gastropod, H. gigantea.

show abstract

Taxonomic and functional heterogeneity of the gill microbiome in a symbiotic coastal mangrove lucinid species

Cited by 49 publications

References 118 publications

Microbial community analysis in the gills of abalones suggested possible dominance of epsilonproteobacterium in Haliotis gigantea

Microbial community analysis in the gills of abalones suggested possible dominance of epsilonproteobacterium in Haliotis gigantea

Extensive Thioautotrophic Gill Endosymbiont Diversity within a Single Ctena orbiculata (Bivalvia: Lucinidae) Population and Implications for Defining Host-Symbiont Specificity and Species Recognition

Peer Review #1 of "Microbial community analysis in the gills of abalones suggested possible dominance of epsilonproteobacterium in Haliotis gigantea (v0.1)"

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