Sexual reproduction in four Caribbean commercial sponges. I. Reproductive cycles and spermatogenesis

Kaye, Heather R.; Reiswig, Henry M.

doi:10.1080/07924259.1991.9672151

Cited by 37 publications

(41 citation statements)

References 18 publications

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“…The presence of MtCK and FlgCK in primitive type sperm was described by Tombes and Shapiro (Tombes and Shapiro, 1989) whereas the potential roles of MtCK and protoflgCK in mediation of the spatial ATP buffering energy transport pathway were proposed by Suzuki and Ellington (Suzuki and Ellington, 2008). The spatial ATP buffering by the CK/PCr system in spermatozoa and sponge choanocytes confirms that the sponge spermatozoa develop from choanocytes during gametogenesis (Kaye and Reiswig, 1991). Furthermore, because of an extreme polarization of the ATP source (mitochondria in the sperm mid-piece) and the ATP sink (dynein ATPases in the flagellum), the CK/PCr system plays a crucial role in sperm motility, creating reaction-diffusion constraints (Suzuki and Ellington, 2008).…”

Section: Discussionmentioning

confidence: 79%

ATP distribution and localization of mitochondria in Suberites domuncula (Olivi 1792) tissue

Lukić-Bilela

Perović-Ottstadt

Walenta

et al. 2011

Journal of Experimental Biology

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SUMMARYThe metabolic energy state of sponge tissue in vivo is largely unknown. Quantitative bioluminescence-based imaging was used to analyze the ATP distribution of Suberites domuncula (Olivi 1792) tissue, in relation to differences between the cortex and the medulla. This method provides a quantitative picture of the ATP distribution closely reflecting the in vivo situation. The obtained data suggest that the highest ATP content occurs around channels in the sponge medulla. HPLC reverse-phase C-18, used for measurement of ATP content, established a value of 1.62mol ATPg -1 dry mass in sponge medulla, as opposed to 0.04mol ATPg -1 dry mass in the cortex, thus indicating a specific and defined energy distribution. These results correlate with the mitochondria localization, determined using primary antibodies against cytochrome oxidase c subunit 1 (COX1) (immunostaining), as well as with the distribution of arginine kinase (AK), essential for cellular energy metabolism (in situ hybridization with AK from S. domuncula; SDAK), in sponge sections. The highest energy consumption seemed to occur in choanocytes, the cells that drive the water through the channel system of the sponge body. Taken together, these results showed that the majority of energetic metabolism in S. domuncula occurs in the medulla, in the proximity of aqueous channels.

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Section: Discussionmentioning

confidence: 79%

ATP distribution and localization of mitochondria in Suberites domuncula (Olivi 1792) tissue

Lukić-Bilela

Perović-Ottstadt

Walenta

et al. 2011

Journal of Experimental Biology

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“…The three cell type transcriptomes generated in this study are clearly distinct from each other ( Choanocytes have been reported to have stem cell-like capacities in several sponge species (Kaye and Reiswig, 1991a;Maldonado and Riesgo, 2008;Funayama et al, 2010;Lanna and Klautau, 2010;Borisenko et al, 2015), with high proliferation rate and dedifferentiation capacities observed in A. queenslandica as well Sogabe et al, 2016).…”

Section: Cell Type Transcriptomes Enriched In Genes Indicative Of Thementioning

confidence: 86%

“…Although it has been suggested that choanocytes have stem cell capacities, these previous observations were made under specific situations such as gametogenesis and regeneration (Anakina and Korotkova, 1989;Kaye and Reiswig, 1991a;Maldonado and Riesgo, 2008;Lanna and Klautau, 2010;Alexander et al, 2015;Borisenko et al, 2015). In A.…”

Section: Discussionmentioning

confidence: 99%

“…Observations under light microscopy shows spermatogenesis in a number of species occurring inside a choanocyte chamber (Anakina and Korotkova, 1989;Barthel and Detmer, 1990;Kaye and Reiswig, 1991a;Gaino et al, 2007;Maldonado and Riesgo, 2008). In some species such as the calcareous sponge Paraleucilla magna, choanocytes are responsible for making both oocytes and spermatozoa (Lanna and Klautau, 2010).…”

Section: Evidence Of Choanocytes As Stem Cellsmentioning

confidence: 99%

“…With potential stem cell capacities of choanocytes observed during gametogenesis and regeneration in multiple species (Anakina and Korotkova, 1989;Kaye and Reiswig, 1991a;Maldonado and Riesgo, 2008;Lanna and Klautau, 2010;Alexander et al, 2015;, as well as dedifferentiation of juvenile choanocyte chambers occurring within 7 days in A. queenslandica , I aimed to further document this process and to elucidate the involvement of choanocytes in the stem cell system. Specifically, I have …”

Section: Evidence Of Choanocytes As Stem Cellsmentioning

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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Setting the foundation for renewal: restoring sponge communities aids the ecological recovery of Florida Bay

et al. 2021

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Coastal ecosystems are constantly buffeted by anthropogenic forces that degrade habitats and alter ecological processes and functions; in turn, this habitat degradation diminishes the ecosystem goods and services on which humans rely. Within the last few decades, the field of restoration ecology has burgeoned into a discipline that marries scientific rigor with functional restoration practice-an idea championed by Pete Peterson and his research. Here, we describe our efforts to restore the hard-bottom sponge communities of Florida Bay, FL (USA)-a once-diverse subtropical lagoon severely degraded by cyanobacteria blooms-and the scientific and practical lessons learned from those efforts. Sponge community restoration yielded insights into basic sponge biology and ecology (e.g., density-dependent growth rates) and hastened the recovery of ecological processes (e.g., rates of sedimentation, structuring of water column characteristics, soundscape productions). Because the results of our initial restoration efforts were promising, our collaboration among academic researchers, natural resource managers, and non-governmental organizations has begun scaling up restoration efforts to re-establish the sponge communities over large areas of degraded hard-bottom to "jump start" the ecological recovery of Florida Bay. Though our efforts show promise for ecological recovery, restoration will require a concerted effort by scientists, resource managers, and citizens to stem the anthropogenic drivers of ecological degradation of this unique South Florida ecosystem.

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Sexual reproduction in four Caribbean commercial sponges. I. Reproductive cycles and spermatogenesis

Cited by 37 publications

References 18 publications

ATP distribution and localization of mitochondria in Suberites domuncula (Olivi 1792) tissue

ATP distribution and localization of mitochondria in Suberites domuncula (Olivi 1792) tissue

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

Setting the foundation for renewal: restoring sponge communities aids the ecological recovery of Florida Bay

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