We present the first mitogenome sequence of the Smoothnose Wedgefish, Rhynchobatus laevis obtained through field sequencing on the MinION handheld sequencer. The mitochondrial genome of R. laevis is 16,560 bp in length and consisted of 13 protein-coding genes (PCGs), 22 tRNA genes, 2 rRNA genes, and a non-coding control region (D-loop). GC content was at 40.1%. The control region was 867 bp in length. Whole mitochondrial genome sequence of R. laevis will enable improved understanding of distribution, abundance, catch and trade rates of the Critically Endangered species.
The epidermis of Chondrichthyan fishes consists of dermal denticles with production of minimal but protein-rich mucus that collectively, influence the attachment and biofilm development of microbes, facilitating a unique epidermal microbiome. Here, we use metagenomics to provide the taxonomic and functional characterization of the epidermal microbiome of the Triakis semifasciata (leopard shark) at three time-points collected across 4 years to identify links between microbial groups and host metabolism. Our aims include (1) describing the variation of microbiome taxa over time and identifying recurrent microbiome members (present across all time-points); (2) investigating the relationship between the recurrent and flexible taxa (those which are not found consistently across time-points); (3) describing the functional compositions of the microbiome which may suggest links with the host metabolism; and (4) identifying whether metabolic processes are shared across microbial genera or are unique to specific taxa. Microbial members of the microbiome showed high similarity between all individuals (Bray–Curtis similarity index = 82.7, where 0 = no overlap, 100 = total overlap) with the relative abundance of those members varying across sampling time-points, suggesting flexibility of taxa in the microbiome. One hundred and eighty-eight genera were identified as recurrent, including Pseudomonas, Erythrobacter, Alcanivorax, Marinobacter, and Sphingopxis being consistently abundant across time-points, while Limnobacter and Xyella exhibited switching patterns with high relative abundance in 2013, Sphingobium and Sphingomona in 2015, and Altermonas, Leeuwenhoekiella, Gramella, and Maribacter in 2017. Of the 188 genera identified as recurrent, the top 19 relatively abundant genera formed three recurrent groups. The microbiome also displayed high functional similarity between individuals (Bray–Curtis similarity index = 97.6) with gene function composition remaining consistent across all time-points. These results show that while the presence of microbial genera exhibits consistency across time-points, their abundances do fluctuate. Microbial functions however remain stable across time-points; thus, we suggest the leopard shark microbiomes exhibit functional redundancy. We show coexistence of microbes hosted in elasmobranch microbiomes that encode genes involved in utilizing nitrogen, but not fixing nitrogen, degrading urea, and resistant to heavy metal.
The epidermal microbiome is a critical element of marine organismal immunity, but the epidermal virome of marine organisms remains largely unexplored. The epidermis of sharks represents a unique viromic ecosystem. Sharks secrete a thin layer of mucus which harbors a diverse microbiome, while their hydrodynamic dermal denticles simultaneously repel environmental microbes. Here, we sampled the virome from the epidermis of three shark species in the family Carcharhinidae: the genetically and morphologically similar Carcharhinus obscurus (n = 6) and Carcharhinus galapagensis (n = 10) and the outgroup Galeocerdo cuvier (n = 15). Virome taxonomy was characterized using shotgun metagenomics and compared with a suite of multivariate analyses. All three sharks retain species-specific but highly similar epidermal viromes dominated by uncharacterized bacteriophages which vary slightly in proportional abundance within and among shark species. Intraspecific variation was lower among C. galapagensis than among C. obscurus and G. cuvier. Using both the annotated and unannotated reads, we were able to determine that the Carcharhinus galapagensis viromes were more similar to that of G. cuvier than they were to that of C. obscurus, suggesting that behavioral niche may be a more prominent driver of virome than host phylogeny.
Characterizations of shark-microbe systems in wild environments have outlined patterns of species-specific microbiomes; however, whether captivity affects these trends has yet to be determined. We used high-throughput shotgun sequencing to assess the epidermal microbiome belonging to leopard sharks (Triakis semifasciata) in captive (Birch Aquarium, La Jolla California born and held permanently in captivity), semi-captive (held in captivity for <1 year in duration and scheduled for release; Scripps Institute of Oceanography, San Diego, CA, USA) and wild environments (Moss Landing and La Jolla, CA, USA). Here, we report captive environments do not drive epidermal microbiome compositions of T. semifasciata to significantly diverge from wild counterparts as life-long captive sharks maintain a species-specific epidermal microbiome resembling those associated with semi-captive and wild populations. Major taxonomic composition shifts observed were inverse changes of top taxonomic contributors across captive duration, specifically an increase of Pseudoalteromonadaceae and consequent decrease of Pseudomonadaceae relative abundance as T. semifasciata increased duration in captive conditions. Moreover, we show captivity did not lead to significant losses in microbial α-diversity of shark epidermal communities. Finally, we present a novel association between T. semifasciata and the Muricauda genus as Metagenomes associated genomes revealed a consistent relationship across captive, semi-captive, and wild populations. Since changes in microbial communities is often associated with poor health outcomes, our report illustrates that epidermally associated microbes belonging to T. semifasciata are not suffering detrimental impacts from long or short-term captivity. Therefore, conservation programs which house sharks in aquariums are providing a healthy environment for the organisms on display. Our findings also expand on current understanding of shark epidermal microbiomes, explore the effects of ecologically different scenarios on benthic shark microbe associations, and highlight novel associations that are consistent across captive gradients.
Marine host-associated microbiomes are affected by a combination of species-specific (e.g., host ancestry, genotype) and habitat-specific features (e.g., environmental physiochemistry and microbial biogeography). The stingray epidermis provides a gradient of characteristics from high dermal denticles coverage with low mucus to reduce dermal denticles and high levels of mucus. Here we investigate the effects of host phylogeny and habitat by comparing the epidermal microbiomes of Myliobatis californica (bat rays) with a mucus rich epidermis, and Urobatis halleri (round rays) with a mucus reduced epidermis from two locations, Los Angeles and San Diego, California (a 150 km distance). We found that host microbiomes are species-specific and distinct from the water column, however composition of M. californica microbiomes showed more variability between individuals compared to U. halleri. The variability in the microbiome of M. californica caused the microbial taxa to be similar across locations, while U. halleri microbiomes were distinct across locations. Despite taxonomic differences, Shannon diversity is the same across the two locations in U. halleri microbiomes suggesting the taxonomic composition are locally adapted, but diversity is maintained by the host. Myliobatis californica and U. halleri microbiomes maintain functional similarity across Los Angeles and San Diego and each ray showed several unique functional genes. Myliobatis californica has a greater relative abundance of RNA Polymerase III-like genes in the microbiome than U. halleri, suggesting specific adaptations to a heavy mucus environment. Construction of Metagenome Assembled Genomes (MAGs) identified novel microbial species within Rhodobacteraceae, Moraxellaceae, Caulobacteraceae, Alcanivoracaceae and Gammaproteobacteria. All MAGs had a high abundance of active RNA processing genes, heavy metal, and antibiotic resistant genes, suggesting the stingray mucus supports high microbial growth rates, which may drive high levels of competition within the microbiomes increasing the antimicrobial properties of the microbes.
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