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Gut microbial diversity and digestive function of an omnivorous shark

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Abstract

The intestinal microbiome of vertebrates has been shown to play a crucial role in their digestive capabilities. This is particularly true for omnivores and herbivores that rely on enteric microbes to digest components of plant material that are indigestible by host-derived enzymes. While studies of microbe-host interactions are becoming more frequent in terrestrial systems, studies of this type are still limited in marine systems, particularly for higher trophic level organisms. Although sharks are largely carnivorous, the bonnethead shark (Sphyrna tiburo) has been identified as an omnivore, given that it assimilates seagrass material in addition to proteinaceous prey items such as crustaceans. The mechanisms by which bonnetheads digest seagrass, including microbial digestion, are still unknown. We use digestive enzyme assays, histological imaging, measurements of microbial fermentation, and 16S rDNA sequencing to explore potential processes by which the bonnethead shark may digest and assimilate plant material. We found evidence of microbial fermentation (as evident by moderate short-chain-fatty-acid concentrations) as well as evidence of greater epithelial surface area in their spiral intestine compared to other gut regions. We identified specific orders of microbes that make up the majority of the bonnethead shark gut microbiome (Vibrionales, Clostridiales, Pseudomonadales, Mycoplasmatales, Rhizobiales, and others), some of which are known, in other organisms, to be involved in the production of enzymes responsible for the breakdown of chitin (found in crustacean shells) and components of cellulose (found in seagrass). Our results highlight that an organism from a stereotypical “carnivorous” group is capable of breaking down seagrass, including potential for some fiber degradation, as well as advances our knowledge of gut microbe community structure in sharks.

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Fig. 1

Adapted from Leigh et al. (2018b)

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All data are presented within the manuscript, figures, supplemental material associated with this manuscript, or on Dryad: https://datadryad.org/stash/share/dJmZXzuwlTU1wUY66IMUO7Ao2mB1iFgrE-DuCI1U5aI

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Acknowledgements

We thank S.Kajiura, W.Chamberlain, S.Hoffmann, B.Bowers, M.Kelley, M.Bergmann, K.Carpenter, K.Sobczak, and the Keys Marine Lab staff for assistance with the fieldwork and the use of field equipment. Thank you to C.Burgett and J.Fourqurean for seagrass acquisition and to S.Sisco and M.Sabando for help in tank maintenance, feedings, and general shark husbandry. Thank you to E. Urena and S. Chen for assisting with lab analyses, K. Whiteson for allowing the use of her gas chromatograph, J. Martiny, C. Weihe, K. Whiteson, and the UCI Microbiome Initiative for assisting with sequencing analyses, and C. Weihe and K. Kohl for analysis advice. This is contribution #252 from the Coastlines and Oceans Division of the Institute of Environment at Florida International University.

Funding

This work was funded by a National Geographic Society Young Explorers Grant, the UCI OCEANS Graduate Research Fellowship, the UCI Newkirk Center Graduate Research Fellowship, the National Science Foundation Graduate Research Fellowship Program, the UCI Graduate Division, and the UCI Microbiome Initiative Pilot Project Award (all to SCL). Funds were also provided by University of California, Irvine laboratory start-up funds (to DPG).

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Conceptualization, SCL, YPP, and DPG. Methodology, SCL and DPG. Investigation, SCL. Writing-original draft, SCL. Writing-reviewing and editing, SCL, YPP, and DPG. Funding acquisition, SCL and DPG.

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Correspondence to Samantha C. Leigh.

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The authors have no conflicts of interest to declare that are relevant to the content of this article.

Ethics

Seagrass was collected with a special activity license issued to James Fourqurean (SAL-15-1754-SR). Sharks were collected with a special activity license issued to Y.P.P. (SAL-16-1825A-SRP). All experiments were approved by FIU IACUC (15-026-CR01).

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Leigh, S.C., Papastamatiou, Y.P. & German, D.P. Gut microbial diversity and digestive function of an omnivorous shark. Mar Biol 168, 55 (2021). https://doi.org/10.1007/s00227-021-03866-3

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