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Trophic Ecology of the Tropical Pacific Sponge Mycale grandis Inferred from Amino Acid Compound-Specific Isotopic Analyses

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Abstract

Many sponges host abundant and active microbial communities that may play a role in the uptake of dissolved organic matter (DOM) by the sponge holobiont, although the mechanism of DOM uptake and metabolism is uncertain. Bulk and compound-specific isotopic analysis of whole sponge, isolated sponge cells, and isolated symbiotic microbial cells of the shallow water tropical Pacific sponge Mycale grandis were used to elucidate the trophic relationships between the host sponge and its associated microbial community. δ15N and δ13C values of amino acids in M. grandis isolated sponge cells are not different from those of its bacterial symbionts. Consequently, there is no difference in trophic position of the sponge and its symbiotic microbes indicating that M. grandis sponge cell isolates do not display amino acid isotopic characteristics typical of metazoan feeding. Furthermore, both the isolated microbial and sponge cell fractions were characterized by a similarly high ΣV value—a measure of bacterial-re-synthesis of organic matter calculated from the sum of variance among individual δ15N values of trophic amino acids. These high ΣV values observed in the sponge suggest that M. grandis is not reliant on translocated photosynthate from photosymbionts or feeding on water column picoplankton, but obtains nutrition through the uptake of amino acids of bacterial origin. Our results suggest that direct assimilation of bacterially synthesized amino acids from its symbionts, either in a manner similar to translocation observed in the coral holobiont or through phagotrophic feeding, is an important if not primary pathway of amino acid acquisition for M. grandis.

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Acknowledgments

We thank Dr. Laura Núñez-Pons (Stazione Zoologica Anton Dohrn) for guidance and assistance in the field, Dr. Ruth Gates (Hawaiʻi Institute of Marine Biology) for invaluable input and use of laboratory facilities, Leon Weaver (Hawaiʻi Institute of Marine Biology) for assistance in the maintenance of experimental facilities, and Jen Davidson (Hawaiʻi Institute of Marine Biology) for technical assistance in the laboratory. This is Hawaiʻi Institute of Marine Biology contribution number 1764 and the School of Ocean and Earth Science and Technology contribution number 10737.

Funding

This study was funded by a grant/cooperative agreement from the National Oceanic and Atmospheric Administration, Project #R/TR-18, which is sponsored by the University of Hawaii Sea Grant Collect Program, SOEST, under Institutional Grant No. #NA14OAR4170071 from NOAA Office of Sea Grant, Department of Commerce. The views expressed herein are those of the authors and do not necessarily reflect the views of NOAA or any of its subagencies.

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Authors and Affiliations

  1. Department of Oceanography, University of Hawai‘i at Mānoa, Honolulu, HI, 96822, USA

    Joy L. Shih & Karen E. Selph

  2. Hawai‘i Institute of Marine Biology, University of Hawai‘i at Mānoa, PO Box 1346, Kāne‘ohe, HI, 96744, USA

    Christopher B. Wall

  3. Department of Earth Sciences, University of Hawai‘i at Mānoa, Honolulu, HI, 96822, USA

    Natalie J. Wallsgrove & Brian N. Popp

  4. Department of Molecular, Cellular and Biomedical Sciences, University of New Hampshire, Durham, NH, 03824, USA

    Michael P. Lesser

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  1. Joy L. Shih
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  2. Karen E. Selph
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  3. Christopher B. Wall
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  4. Natalie J. Wallsgrove
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  6. Brian N. Popp
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Correspondence to Brian N. Popp.

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Shih, J.L., Selph, K.E., Wall, C.B. et al. Trophic Ecology of the Tropical Pacific Sponge Mycale grandis Inferred from Amino Acid Compound-Specific Isotopic Analyses. Microb Ecol 79, 495–510 (2020). https://doi.org/10.1007/s00248-019-01410-x

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