Ingestion, digestion, and egestion in Spongilla lacustris (Porifera, Spongillidae) after pulse feeding with Chlamydomonas reinhardtii (Volvocales)

Imsiecke, Georg

doi:10.1007/bf00403314

Cited by 70 publications

(65 citation statements)

References 34 publications

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“…I then analysed the expression patterns of these genes across transcriptome profiles of choanocytes, pinacocytes and archaeocytes that were generated from adult conspecifics that did not receive any bacterial treatments. The involvement of these three cell-types in mediating ingestion and subsequent processing of bacteria has previously been documented in other demosponges species (Imsiecke 1993;Maldonado, et al 2010). Additionally, ingested bacteria were observed in the choanocytes, choanocyte-associated amoeboid cells and archaeocytes of A. queenslandica in the present study.…”

Section: Genes Putatively Involved In Regulating Sponge-bacteria Intesupporting

confidence: 83%

Deciphering the genomic toolkit underlying animal-bacteria interactions – insights through the demosponge Amphimedon queenslandica

Yuen¹

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All animals are inhabited by bacteria, and maintaining homeostasis in the multicellular environment of the host involves the complex balancing act of promoting the survival of symbionts while defending against intruders. Sponges (Porifera), in addition to housing diverse bacterial symbiont assemblages, also rely on bacteria filtered from the water column for nutrition. My research uses the genome-enabled demosponge, Amphimedon queenslandica, a member of one of the earliest-diverging animal phyletic lineages, as an experimental platform to investigate the genomic toolkit underpinning animal-bacteria interactions. Using comparative bioinformatics tools, I characterised a surprisingly large and complex repertoire of innate immune receptors from the NLR family of genes encoded in the A. queenslandica genome. I then used a high throughput RNAseq approach to profile the sponge's global transcriptomic response to foreign versus its own native bacteria. Conserved metazoan innate immune pathways were activated in response to both foreign and native bacteria. However, only the native bacteria elicited the expression of a more extensive suite of signalling pathways, involving TGF-β signalling and the transcription factors NF-κB and FoxO. Upregulation of the nutrient sensor AMPK in all treatments along with immune signalling genes, which all regulate FoxO activity, further suggests an interplay between metabolic homeostasis and immunity. Finally, I used microscopy to track the cellular-level processing of the different bacteria by the sponge. Consistent with the observed transcriptional response, the native bacteria were ingested by archaeocytes more rapidly than the foreign bacteria. The slower processing of foreign bacteria also correlated with the expression of numerous Nrf2-associated detoxification genes, indicative of cellular stress, only in response to foreign bacteria.iii Deciphering the genomic tool-kit underlying animal-bacteria interactions

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Section: Genes Putatively Involved In Regulating Sponge-bacteria Intesupporting

confidence: 83%

Deciphering the genomic toolkit underlying animal-bacteria interactions – insights through the demosponge Amphimedon queenslandica

Yuen¹

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“…Reiswig 1971, Pile et al 1996, Pile 1997, as well as larger organisms, including yeast cells, heterotrophic and autotrophic flagellates, diatoms, and ciliates (e.g. Frost 1978, Imsiecke 1993, Pile et al 1996, Ribes et al 1999. Nevertheless, the filtering system is rather specialized in retaining picoplankton (size range 0.1 to 2 µm) with maximum efficiency, and somewhat less efficiently nanoplankton (2 to 20 µm), which together provide the bulk of the diet (e.g.…”

Section: Introductionmentioning

confidence: 99%

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

Maldonado¹,

Zhang²,

Cao³

et al. 2010

Mar. Ecol. Prog. Ser.

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Sponges have traditionally been viewed as rather unselective filter feeders, and therefore as potential biofilters to remediate microbial water pollution. Here we show that the assumed connection between the ability of sponges to feed on microbes and the potential biotechnological use of such an ability to reduce microbial pollution is more complex than assumed. In a laboratory feeding experiment combined with a transmission electron microscopy study, we assessed the potential of the marine sponge Hymeniacidon perlevis to ingest and digest 3 common pathogenic microbes occurring in coastal waters: 2 bacteria (Escherichia coli and Vibrio anguillarum), and 1 marine yeast Rhodotorula sp. All 3 microbes were ingested by the sponge, but selectively, at different rates and following different cellular mechanisms. Yeast cells were processed very atypically by the sponge. Differences in the ingestion and digestion pathways led to large differences in the effectiveness of the sponge to remove the microbes. While sponge grazing reduced the concentration of E. coli and Rhodotorula sp. to levels far below the initial values, sponges were ineffective in abating concentrations of the most infective bacterium, V. anguillarum. This bacterium, which was digested more slowly than E. coli, proliferated in the experimental flasks at much higher rates than it was grazed. These findings raise the question whether sponges are suitable for bioremediation of microbial pollution, since selective or preferential ingestion of certain bacteria by sponges may end up fueling growth of those grazed less, such as Vibrio spp.

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“…This aquiferous system comprises the main structure of the sponge body and is necessary for filter feeding, respiration and excretion via incurrent and excurrent canals (Leys and Hill, 2012;. Food capture generally occurs through the choanocytes by water flow generated by the collar and flagellum (Simpson, 1984;Imsiecke, 1993;Leys and Eerkes-Medrano, 2006), although other epithelial cells (i.e. endopinacocytes lining the canals, exopinacocytes of the surface epithelial layer) have been demonstrated to have phagocytic capacities as well (Willenz and Van de Vyver, 1982;Imsiecke, 1993).…”

Section: Overviewmentioning

confidence: 99%

“…Food capture generally occurs through the choanocytes by water flow generated by the collar and flagellum (Simpson, 1984;Imsiecke, 1993;Leys and Eerkes-Medrano, 2006), although other epithelial cells (i.e. endopinacocytes lining the canals, exopinacocytes of the surface epithelial layer) have been demonstrated to have phagocytic capacities as well (Willenz and Van de Vyver, 1982;Imsiecke, 1993). From Chapter 4, it is now likely that choanocytes play an essential role in the sponge in terms of both growth and maintenance, not only as a feeding cell.…”

Section: Overviewmentioning

confidence: 99%

“…However, there have been multiple observations on the food transfer between choanocytes and amoeboid cells (Simpson, 1984;Imsiecke, 1993), as well as between amoeboid cells and other cell types (Willenz and Van de Vyver, 1984;, suggesting food particle transfer between cells occur via vesicular transport. What then, would be the benefit of mesohyl cells becoming choanocytes themselves, if transporting food particles between cell types is commonly done by vesicles?…”

Section: What Is the Function Of Recruitment Of Cells Into Choanocytementioning

confidence: 99%

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The biology of choanocytes and choanocyte chambers and their role in the sponge stem cell system

Sogabe¹

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Metazoan multicellularity required the evolution of cellular processes such as cell differentiation, cell-cell adhesion and communication, along with complex gene regulatory networks and the emergence of a stem cell system. Choanocytes, the collared feeding cells in sponges, have been extensively compared to choanoflagellates, the closest sister group to metazoans due to their morphological similarities and their capacity to form multicellular structures. Recently available genomic and transcriptomic data alongside observational studies on the multicellular colonies in choanoflagellate Salpingoeca rosetta, revealed many genes shared with metazoans are upregulated only when the S. rosetta cells form colonies, while there has been little progress made on understanding the development of sponge choanocyte chambers. Choanocytes have also been suggested as playing a part in the sponge stem cell system, but again, there is limited knowledge on their general biology. To expand our understanding on this unique feeding cell that has potential stem cell capacities as well as a long-suggested homology with a closely related unicellular holozoan, I investigated molecular mechanisms underlying the development and maintenance of choanocyte chambers in the demosponge Amphimedon queenslandica.During my PhD, I have documented the formation and maintenance of choanocyte chambers in detail using cell trackers and proliferation assays, showing their dynamic nature in the sponge body as part of the stem cell system. Contrary to previous studies in sponges as well as choanoflagellates, I found that choanocyte chamber development is not always clonal, and a chamber is not always comprised of a clonal cell population. After metamorphosis, choanocytes in these chambers are also capable of dedifferentiating into archeocytes, which can subsequently differentiate into multiple cell types including new choanocyte chambers. I propose that choanocyte chambers in A. queenslandica are playing a central role in the stem cell system, increasing and maintaining the stem cell population. I have also identified genes uniquely expressed in choanocytes, as well as archeocytes (primary stem cells) and pinacocytes (epithelial cells) by manually isolating these cell types from adult sponges, which was sequenced using CEL-Seq. From this, I have obtained a reliable transcriptome for three major cell types comprising the sponge body plan. A number of analyses on the A. queenslandica choanocyte transcriptome and publicly available choanoflagellate datasets, show no strong evidence of a shared gene repertoire between choanocytes and choanoflagellates. This thesis provides a detailed documentation of choanocyte chambers and their biology in the sponge body, along with developing a number of lab-based III techniques and cell-type specific transcriptomes to be utilized for further investigation on the sponge stem cell system and the evolution of metazoan multicellularity.

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Ingestion, digestion, and egestion in Spongilla lacustris (Porifera, Spongillidae) after pulse feeding with Chlamydomonas reinhardtii (Volvocales)

Cited by 70 publications

References 34 publications

Deciphering the genomic toolkit underlying animal-bacteria interactions – insights through the demosponge Amphimedon queenslandica

Deciphering the genomic toolkit underlying animal-bacteria interactions – insights through the demosponge Amphimedon queenslandica

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

The biology of choanocytes and choanocyte chambers and their role in the sponge stem cell system

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