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

Doane, Michael P.; Johnson, Colton J.; Johri, Shaili; Kerr, Emma N.; Morris, Megan M.; Desantiago, Ric; Turnlund, Abigail C.; Goodman, Asha; Mora, Maria; Lima, Laís Oliveira; Nosal, Andrew P.; Dinsdale, Elizabeth A.

doi:10.1007/s00248-022-01969-y

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

Journal Article · 06 February 2022 · Microbial Ecology

DOI: https://doi.org/10.1007/s00248-022-01969-y · OSTI ID:1883018

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^[3]; Kerr, Emma N. ^[1];

^[4]; Desantiago, Ric ^[2]; Turnlund, Abigail C. ^[5]; Goodman, Asha ^[2]; Mora, Maria ^[2];

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Flinders Univ., Adelaide, SA (Australia)
San Diego State Univ., CA (United States)
Stanford Univ., Pacific Grove, CA (United States)
Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
Univ. of Queensland, St. Lucia, QLD (Australia)
Univ. of San Diego, San Diego, CA (United States); Univ. of California, San Diego, La Jolla, CA (United States)

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.

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Research Organization:: Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)

Sponsoring Organization:: National Science Foundation (NSF); USDOE National Nuclear Security Administration (NNSA)

Grant/Contract Number:: AC52-07NA27344

OSTI ID:: 1883018

Report Number(s):: LLNL-JRNL-826714; 1041428

Journal Information:: Microbial Ecology, Journal Name: Microbial Ecology Journal Issue: 2 Vol. 85; ISSN 0095-3628

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

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Similar bacterial communities on healthy and injured skin of black tip reef sharks Pogoreutz, Claudia; Gore, Mauvis; Perna, Gabriela figshare https://doi.org/10.6084/m9.figshare.c.4668008	collection	January 2019
The skin microbiome of elasmobranchs follows phylosymbiosis, but in teleost fishes, the microbiomes converge Doane, Michael P.; Morris, Megan M.; Papudeshi, Bhavya figshare https://doi.org/10.6084/m9.figshare.c.5020859	collection	January 2020
Highly abundant core taxa in the blow within and across captive bottlenose dolphins provide evidence for a temporally stable airway microbiota Vendl, Catharina; Nelson, Tiffanie; Ferrari, Belinda figshare https://doi.org/10.6084/m9.figshare.c.5263312	collection	January 2021
A mixed community of skin microbiome representatives influences cutaneous processes more than individual members Loomis, Kristin H.; Wu, Susan K.; Ernlund, Amanda figshare https://doi.org/10.6084/m9.figshare.c.5279205	collection	January 2021
Elasmobranch microbiomes: emerging patterns and implications for host health and ecology Perry, Cameron T.; Pratte, Zoe A.; Clavere-Graciette, Ana figshare https://doi.org/10.6084/m9.figshare.c.5620252	collection	January 2021
Description of the microbiota in epidermal mucus and skin of sharks (Ginglymostoma cirratum and Negaprion brevirostris) and one stingray (Hypanus americanus) Caballero, Susana; Galeano, Ana Maria; Lozano, Juan Diego PeerJ, Vol. 8 https://doi.org/10.7717/peerj.10240	journal	December 2020
Aura-biomes are present in the water layer above coral reef benthic macro-organisms Walsh, Kevin; Haggerty, J. Matthew; Doane, Michael P. PeerJ, Vol. 5 https://doi.org/10.7717/peerj.3666	journal	January 2017
Skin bacterial diversity is higher on lizards than sympatric frogs in tropical Australia Weitzman, Chava L.; Gibb, Karen; Christian, Keith PeerJ, Vol. 6 https://doi.org/10.7717/peerj.5960	journal	November 2018