Bacterial Uptake by the Marine Sponge Aplysina aerophoba

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 x 10(6) bacteria (g sponge wet weight)(-1) h(-1), whereas the retention of sponge symbionts was lower by nearly two orders of magnitude [5.37 x 10(4) 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.

Selective feeding by sponges on pathogenic microbes: a reassessment of potential for abatement of microbial pollution

“…In the case of Vibrio anguillarum, the occurrence of a flagellum, which is likely to be beating within the choanocyte chambers during the process of phagocytosis, might well complicate the engulfing by the choanocytes. However, Wehrl et al (2007) reported that retentions rates of hyperflagellated and hypoflagellated Vibrio mutants were similar to that of the respective wild-type strain. Therefore, it has to be considered that choanocytes are actually able to discriminate bacteria by perceiving characteristic wall compounds, as suggested by Wehrl et al (2007).…”

“…However, a few studies have clearly demonstrated that at least some sponges may perform a size-independent selection of the ingested microbes (e.g. Frost 1976, 1980b, Van de Vyver et al 1990, Yahel et al 2006, Wehrl et al 2007). Likewise, the outcome of our experiment supports that feeding in Hymeniacidon perlevis is a selective process.…”

Complex interactions between marine sponges and their symbiotic microbial communities

“…Sponge and microbial cell separations-Methods for cell separation were adapted from Wehrl et al (2007). Frozen sponge specimens (6 to 10 cm long) were thawed at 4uC, weighed to the nearest 0.01 g, and minced into small pieces using a sterile razor blade.…”

Functional genomic signatures of sponge bacteria reveal unique and shared features of symbiosis

“…AR proteins have also been recently shown to be secreted by the intracellular pathogens Legionella pneumophila and Coxiella burnetii and to interfere with the microtubule-dependent vascular transport of host cells, hence blocking the normal progression of phagocytosis (Pan et al, 2008). As uptake of food bacteria by sponge cells is also mediated by phagocytosis (Wehrl et al, 2007), the sponge-specific AR and TPR proteins reported in this study could possibly represent a mechanism by which symbiotic bacteria avoid digestion, and could explain the long-standing question of how food and symbionts are discriminated by the sponge (Wilkinson et al, 1984).…”