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Bacterial Uptake by the Marine Sponge Aplysina aerophoba

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Abstract

Sponges (Porifera) are filter feeders that take up microorganisms from seawater and digest them by phagocytosis. At the same time, many sponges are known to harbor massive consortia of symbiotic microorganisms, which are phylogenetically distinct from those in seawater, within the mesohyl matrix. In the present study, feeding experiments were performed to investigate whether phylogenetically different bacterial isolates, hereafter termed “food bacteria,” microbial seawater consortia, and sponge symbiont consortia are taken up and processed differently by the host sponge. Aplysina aerophoba retained high numbers of bacterial isolates and microbial seawater consortia with rates of up to 2.76 × 106 bacteria (g sponge wet weight)–1 h–1, whereas the retention of sponge symbionts was lower by nearly two orders of magnitude [5.37 × 104 bacteria (g sponge wet weight)−1 h–1]. In order to visualize the processing of a food bacterium within sponge tissues, the green fluorescent protein-labeled Vibrio strain MMW1, which had originally been isolated from A. aerophoba, was constructed. Incubation of this strain with A. aerophoba and subsequent visualization in tissue cryosections showed its presence in the choanocytes and/or endopinacocytes lining the canals but, unlike latex beads, not in deeper regions of the mesohyl, which suggests digestion of the bacteria upon contact with the host. Denaturing gradient gel electrophoresis (DGGE) was performed on the incubation seawater to monitor the changes in phylogenetic composition after incubation of the sponge with either seawater or sponge symbiont consortia. However, the DGGE experiment provided no evidence for selective processing of individual lineages by the host sponge. In conclusion, this study extends early studies by Wilkinson et al. (Proc R Soc London B 220:519–528, 1984) that sponges, here A. aerophoba, are able to differentiate between food bacteria and their own bacterial symbionts.

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Acknowledgments

We gratefully acknowledge the marine operations personnel at the Laboratoire Arago for help during sponge collection and H. Moreau for sharing laboratory space and equipment (Banyuls-sur-Mer, France). We thank S. Schmitt for laboratory assistance and valuable discussions, E. Strom for mathematical support, K. Heuner for help with the construction of the GFP-labeled Vibrio strain MMW1 (all University of Würzburg), and D. Millikan (University of Hawaii) for the supply of Vibrio flagellar mutants. Financial support for this work was provided by the SFB567 to U. Hentschel and M. Steinert.

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Wehrl, M., Steinert, M. & Hentschel, U. Bacterial Uptake by the Marine Sponge Aplysina aerophoba . Microb Ecol 53, 355–365 (2007). https://doi.org/10.1007/s00248-006-9090-4

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