Oogenesis and spermatogenesis in Paraleucilla magna (Porifera, Calcarea)

Lanna, Emílio; Klautau, Michelle

doi:10.1007/s00435-010-0117-5

Cited by 35 publications

(61 citation statements)

References 31 publications

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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: 87%

“…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%

“…In some species such as the calcareous sponge Paraleucilla magna, choanocytes are responsible for making both oocytes and spermatozoa (Lanna and Klautau, 2010). However, as there have been reports of spermatogenesis from archeocytes as well (Boury-Esnault et al, 1999;Leys and Ereskovsky, 2006), gametogenesis in sponges appears to vary greatly depending on the species.…”

Section: Evidence Of Choanocytes As Stem Cellsmentioning

confidence: 95%

“…Although it was generally considered that archeocytes are primarily responsible for the regeneration capacity of sponges (Agata et al, 2006;Müller, 2006), there is increasing evidence from many sponge species suggesting the involvement of multiple cell types, and their high relatively high plasticity even as differentiated cells. Choanocytes have high proliferation rates in many species (Tanaka and Watanabe, 1984;De Goeij et al, 2009;Alexander et al, 2014), along with a capacity to dedifferentiate in A. queenslandica , as well as their involvement in gametogenesis (Lanna and Klautau, 2010) and regeneration through transdifferentiation in some species (Alexander et al, 2015;Borisenko et al, 2015).…”

Section: Gene Expression Analysis Using Expression Quartiles: a Potenmentioning

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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Section: Cell Type Transcriptomes Enriched In Genes Indicative Of Thementioning

confidence: 87%

Section: Discussionmentioning

confidence: 99%

Section: Evidence Of Choanocytes As Stem Cellsmentioning

confidence: 95%

Section: Gene Expression Analysis Using Expression Quartiles: a Potenmentioning

confidence: 99%

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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Anatomy and ultrastructure of the tropical sponge Cladocroce caelum (Haplosclerida, Demospongiae)

Hora

Cavalcanti

Lanna

2018

Journal of Morphology

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The main characteristic of sponges (Porifera) is the presence of the aquiferous system-a system formed by canals and choanocyte chambers, in which the sponges carry out most of their physiological functions. Despite of the importance for the biology of the group, the knowledge about this structure is still incipient, even when morphological investigations are taken in account.Here, we investigated the anatomy and ultrastructure of the tropical demosponge Cladocroce caelum (Haplosclerida, Demospongiae) using light and electron microscopy. In the studied region, specimens of this species were repent or repent-branched, possessing one to several oscula. A uniform and reduced atrium was found just below each osculum. There was a thin ectosome and the choanosome presented meager mesohyl, but a high number of choanocyte chambers. The choanocyte chambers were rounded, and, as in other haplosclerids, they are found separated from the mesohyl by endopinacocytes, "hanging" in the inhalant canals. Even though the utility of the general organization of the aquiferous system has been advocated as a possible tool to understand the phylogeny of the group, we found that these characters might not be as useful as expected. The size of the particles ingested by the sponge and the amount of bacteria to sustain their bodies are discussed. In addition, we found that the density of choanocyte chambers was reduced when the specimens were carrying out the spermatogenesis, indicating that the reproduction may impair the filtering activity of the sponge. Our findings consist in a first step to better comprehend the physiology, development, and adaptation to the environmental conditions where the species is found.

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Ultrastructure of oogenesis in two tropical oviparous Demospongiae (Porifera): Cinachyrella apion and Tethya maza

Vasconcellos¹,

Leys

Lanna³

2023

Journal of Morphology

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Reproduction is a key step for propagation of any species. Consequently, gametogenesis is crucial, as it links one generation to the other. Oogenesis is influenced by different factors, but it is usually related to the quality and quantity of the food and the capacity of the female to convert these resources into egg production. In Demospongiae (Porifera), oocytes vary in several aspects (e.g., origin, size, and vitellogenic pathways). However, data on oocyte morphology is still fragmentary, and the ultrastructural organization of reproductive cells has been investigated only in a few species, mainly of viviparous sponges. Here, we aimed to comprehend the oogenesis of two tropical oviparous demosponges (Cinachyrella apion and Tethya maza) using light and electron microscopy. In both species, oocytes seemed to originate from archaeocytes. Oocytes of C. apion were surrounded by a collagenous matrix and nurse cells containing many lipid vesicles. The increase of biosynthetic organelles, concomitantly with the presence of yolk vesicle in the ooplasm, indicated that the vitellogenesis was carried out through the mixed pathway. The oocytes of T. maza were surrounded by a follicle cell membrane and nurse cells containing yolk vesicles. The absence of characteristic biosynthetic organelles in the egg of this species indicated that vitellogenesis occured through the heterosynthetic pathway. The oogenesis of C. apion is similar to other species of the genus, while the follicle membrane and nurse cells surrounding the oocytes of T. maza are not observed in any other species of Tethya. These accessory cells were considered to have a trophic role during the oogenesis of the studied species. Moreover, the presence of these accessory cells may have ecological significance, as they accelerate the egg's production through trophic support of the growing oocyte.

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Oogenesis and spermatogenesis in Paraleucilla magna (Porifera, Calcarea)

Cited by 35 publications

References 31 publications

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

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

Anatomy and ultrastructure of the tropical sponge Cladocroce caelum (Haplosclerida, Demospongiae)

Ultrastructure of oogenesis in two tropical oviparous Demospongiae (Porifera): Cinachyrella apion and Tethya maza

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