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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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Journal Microb Ecol
Date 2019 Jul 18
PMID 31312870
Citations 5
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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. δN and δC 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 δN 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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References
1.
Pile A, Grant A, Hinde R, Borowitzka M . Heterotrophy on ultraplankton communities is an important source of nitrogen for a sponge-rhodophyte symbiosis. J Exp Biol. 2003; 206(Pt 24):4533-8. DOI: 10.1242/jeb.00698. View

2.
LaJeunesse T, Parkinson J, Gabrielson P, Jeong H, Reimer J, Voolstra C . Systematic Revision of Symbiodiniaceae Highlights the Antiquity and Diversity of Coral Endosymbionts. Curr Biol. 2018; 28(16):2570-2580.e6. DOI: 10.1016/j.cub.2018.07.008. View

3.
Larsen T, Taylor D, Leigh M, OBrien D . Stable isotope fingerprinting: a novel method for identifying plant, fungal, or bacterial origins of amino acids. Ecology. 2010; 90(12):3526-35. DOI: 10.1890/08-1695.1. View

4.
Fiore C, Labrie M, Jarett J, Lesser M . Transcriptional activity of the giant barrel sponge, Xestospongia muta Holobiont: molecular evidence for metabolic interchange. Front Microbiol. 2015; 6:364. PMC: 4412061. DOI: 10.3389/fmicb.2015.00364. View

5.
Wang G, Yoon S, Lefait E . Microbial communities associated with the invasive Hawaiian sponge Mycale armata. ISME J. 2008; 3(3):374-7. DOI: 10.1038/ismej.2008.107. View