Stem cells in Nanomia bijuga (Siphonophora), a colonial animal with localized growth zones

Abstract

BackgroundSiphonophores (Hydrozoa) have unparalleled colony-level complexity, precision of colony organization, and functional specialization between zooids (i.e., the units that make up colonies). Previous work has shown that, unlike other colonial animals, most growth in siphonophores is restricted to one or two well-defined growth zones that are the sites of both elongation and zooid budding. It remained unknown, however, how this unique colony growth and development is realized at the cellular level.ResultsTo understand the colony-level growth and development of siphonophores at the cellular level, we characterize the distribution of proliferating cells and interstitial stem cells (i-cells) in the siphonophore Nanomia bijuga. Within the colony, we find evidence that i-cells are present at the tip of the horn, the structure within the growth zone that gives rise to new zooids. Co-localized gene expression of vasa-1, pl10, piwi, nanos-1, and nanos-2 suggests that i-cells persist in the youngest zooid buds and that i-cells become progressively restricted to specific regions within the zooids until they are mostly absent from the oldest zooids. The examined genes remain expressed in gametogenic regions. No evidence for i-cells is found in the stem between maturing zooids. Domains of high cell proliferation include regions where the examined genes are expressed, but also include some areas in which the examined genes were not expressed such as the stem within the growth zones. Cell proliferation in regions devoid of vasa-1, pl10, piwi, nanos-1, and nanos-2 expression indicates the presence of mitotically active epithelial cell lineages and, potentially, progenitor cell populations.ConclusionsWe provide the first evidence for i-cells in a siphonophore. Our findings suggest maintenance of i-cell populations at the sites of growth zones and that these sites are the main source of i-cells. This restriction of stem cells to particular regions in the colony, in combination with localized budding and spatial patterning during pro-bud subdivision, may play a major role in facilitating the precision of siphonophore growth. Spatially restricted maintenance of i-cells in mature zooids and absence of i-cells along the stem may explain the reduced developmental plasticity in older parts of the colony.Electronic supplementary materialThe online version of this article (doi:10.1186/s13227-015-0018-2) contains supplementary material, which is available to authorized users.

The histology of Nanomia bijuga (Hydrozoa: Siphonophora)

“…Specimens were collected in Monterey Bay on Sep 29, 2012 via blue‐water diving from a depth of 10–20 m. The specimens examined here were also used for the histological examinations of stem cells by Siebert et al (). Slides with representative thick sections and three additional whole N. bijuga specimens collected on the same dive have been deposited in the Museum of Comparative Zoology at Harvard, accession numbers IZ 50112–IZ 50016.…”

“…Siebert et al () quantified differential gene expression between zooids using RNA‐seq, and demonstrated the first in situ mRNA hybridizations in the species. Siebert et al () described the distribution of stem cells throughout N. bijuga , finding that they are restricted to the growth zones, young zooids, and particular regions of some mature zooids.…”

Sex, polyps, and medusae: Determination and maintenance of sex in cnidarians

“…If these observations hold up for other hydrozoans, this model might help us understand phenomena in more complex colonies, such as the siphonophore Nanomia bijuga , a colonial hydrozoan with male and female gonozooids arranged in a highly organized spatial pattern (Totton, ). Molecular markers indicate localized growth zones in N. bijuga as the source of ISCs, which are incorporated into newly forming zooid buds within the growth zones (Siebert et al, ). The predictable arrangement of male and female zooids indicates that the somatic cells of the newly forming zooids influence whether male or female interstitial cells colonize a new reproductive zooids, or at least influence whether eggs or sperm are produced in a particular zooid.…”

PL10 DEAD‐Box Protein is Expressed during Germ Cell Differentiation in the Reptile Podarcis sicula (Family Lacertidae)

“…In recent years, a number of “germ line factors” driving germ cell differentiation in both sexes have been identified in several species. Among these factors, the genes of DDX4/Vasa and Ded1/DDX3 subfamilies have been investigated in several invertebrates and vertebrates (Raz, ; Leclère et al., ; Sharma and Jankowsky, ; Kozin and Kostyuchenko, ; Siebert et al., ; Fierro‐Constaín et al., ). These genes encode for DEAD‐box ATP‐dependent RNA helicases (Linder et al., ) and proteins found in all eukaryotes and most prokaryotes (e.g., Schmid and Linder, ; Fujiwara et al., ; Komiya et al., ; Fabioux et al., ; Zhou et al., ).…”

“…DDX4/Vasa proteins are expressed in both male and female germ cells (Lasko and Ashburner, ) and are essential in gametogenesis and germ cell specification during embryogenesis (Raz, ). Nonetheless, in some animals, DDX4/Vasa proteins are also expressed in stem cells of diverse origin, in which they contribute to cell cycle and developmental regulation (Leclère et al., ; Kozin and Kostyuchenko, ; Siebert et al., ; Yajima and Wessel, ; Fierro‐Constaín et al., ). In other animals, their expression appears to be restricted to the germ cell lineage (Zhou et al., ).…”