The Epidermal Microbiome Within an Aggregation of Leopard Sharks (Triakis semifasciata) Has Taxonomic Flexibility with Gene Functional Stability Across Three Time-points

Abstract

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.

Epidermal Microbiomes of Leopard Sharks (Triakis semifasciata) Are Consistent across Captive and Wild Environments

“…The approximate 200 mL of captured microbe was collected on a Sterivex (Millipore, Inc.), where one Sterivex per individual was obtained each collection date. The blunt edge syringe has been used many times to collect microbes from underwater organisms [ 2 , 3 , 4 , 23 ] and has the advantage of dislodging the microbiome from in and under the dermal denticles, without the disrupting the host tissue and becoming inoculated with products such as melanin [ 2 , 3 , 5 , 24 ].…”

“…The eukaryotic host and the respective microbiome has been reclassified as a metaorganism, representing a functional system that adapts to changing environments and external threats by cultivating a synergistic interdependence with microscopic symbionts [ 1 ]. The epidermal microbiome of the marine metaorganism reflects both environmental conditions and host-microbiome interdependent effects, in addition to directly interfacing with seawater, while remaining distinct from the pool of microbes in the water column [ 2 , 3 , 4 , 5 ]. The epidermal microbiomes belonging to triple fin fish ( Forsterygion capito ) experiencing polluted conditions, for example, have lower levels of biodiversity compared to fish residing in pristine environments [ 6 ].…”

Elasmobranchs Exhibit Species-Specific Epidermal Microbiomes Guided by Denticle Topography

“…Therefore, Staphylococcus associations may be selectively favored by the unique combination of decreased denticle coverage and increased mucus production characteristic of C. ventriosum . To build upon this theory, we posit the enhanced denticle overlap and less pronounced riblet elevation in conjunction with minimal but protein-rich mucus of T. semifasciata skin, provides a conducive surface for Staphylococcus to colonize 47 , while C. ventriosum offers the greatest opportunity for providing mucus production as a function of exposed epidermis. Last, the distinct structural environment of H. francisci’s dermal denticles, characterized by pronounced riblets and troughs, may be less hospitable to Staphylococcus , despite the potential assistance provided by mucus produced from a more exposed epidermal environment.…”

Decoding the Transcriptome of Sharks, Rays, and Chimaeras: Insights into Their Physiology, Morphology, Evolution, and Biomedical Applications

“…Here, we critically review the current knowledge and available resources about the transcriptomes of cartilaginous jawed fishes, which in line with other sequencing techniques and data, such as genomics [25][26][27], proteomics [28,29] and microbiomes [30][31][32], is likely to foster research in this fish class. We collected detailed information regarding the available sequences from the SRA NCBI Database and from literature, aiming to understand the state-of-art of Chondrichthyes' transcriptomics.…”