Nitric oxide (NO) is a ubiquitous gaseous messenger, but we know little about its early evolution. Here, we analyzed NO synthases (NOS) in four different species of placozoans—one of the early-branching animal lineages. In contrast to other invertebrates studied,
Hidden cell diversity in Placozoa: ultrastructural insights from Hoilungia hongkongensis
From a morphological point of view, placozoans are among the most simple free-living animals. This enigmatic phylum is
critical for our understanding of the evolution of animals and their cell types. Their millimeter-sized, disc-like bodies consist
of only three cell layers that are shaped by roughly seven major cell types. Placozoans lack muscle cells and neurons but are
able to move using their ciliated lower surface and take up food in a highly coordinated manner. Intriguingly, the genome of
Trichoplax adhaerens, the founding member of the enigmatic phylum, has disclosed a surprising level of genetic complexity.
Moreover, recent molecular and functional investigations have uncovered a much larger, so-far hidden cell-type diversity.
Here, we have extended the microanatomical characterization of a recently described placozoan species—Hoilungia hongkongensis.
In H. hongkongensis, we recognized the established canonical three-layered placozoan body plan but also came
across several morphologically distinct and potentially novel cell types, among them novel gland cells and “shiny spheres”-
bearing cells at the upper epithelium. Thus, the diversity of cell types in placozoans is indeed higher than anticipated
more »
« less
- Award ID(s):
- 1645219
- NSF-PAR ID:
- 10287243
- Date Published:
- Journal Name:
- Cell and Tissue Research
- ISSN:
- 0302-766X
- Page Range / eLocation ID:
- 1-15
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Abstract Trichoplax andHoilungia have three distinct NOS genes, including PDZ domain-containing NOS. Using ultra-sensitive capillary electrophoresis assays, we quantified nitrites (products of NO oxidation) andl -citrulline (co-product of NO synthesis froml -arginine), which were affected by NOS inhibitors confirming the presence of functional enzymes inTrichoplax . Using fluorescent single-molecule in situ hybridization, we showed that distinct NOSs are expressed in different subpopulations of cells, with a noticeable distribution close to the edge regions ofTrichoplax . These data suggest both the compartmentalized release of NO and a greater diversity of cell types in placozoans than anticipated. NO receptor machinery includes both canonical and novel NIT-domain containing soluble guanylate cyclases as putative NO/nitrite/nitrate sensors. Thus, althoughTrichoplax andHoilungia exemplify the morphologically simplest free-living animals, the complexity of NO-cGMP-mediated signaling in Placozoa is greater to those in vertebrates. This situation illuminates multiple lineage-specific diversifications of NOSs and NO/nitrite/nitrate sensors from the common ancestor of Metazoa and the preservation of conservative NOS architecture from prokaryotic ancestors. -
Placozoans are essential reference species for understanding the origins and evolution of the animal organization. However, little is known about their life strategies in natural habitats. Here, by establishing long-term culturing for four species of Trichoplax and Hoilungia, we extend our knowledge about feeding and reproductive adaptations relevant to their ecology and immune mechanisms. Three modes of population growth depended upon feeding sources, including induction of social behaviors and different reproductive strategies. In addition to fission, representatives of all haplotypes produced ‘swarmers,’ which could be formed from the lower epithelium (with greater cell- type diversity) as a separate asexual reproduction stage. In aging culture, we reported the formation of specialized structures (‘spheres’) from the upper cell layer as a part of the innate immune defense response with the involvement of fiber cells. Finally, we showed that regeneration could be a part of the adaptive reproductive strategies in placozoans and a unique model for regenerative biology in general.more » « less
-
Hydractinia is a colonial marine hydroid that exhibits remarkable biological properties, including the capacity to regenerate its entire body throughout its lifetime, a process made possible by its adult migratory stem cells, known as i-cells. Here, we provide an in-depth characterization of the genomic structure and gene content of two Hydractinia species, H. symbiolongicarpus and H. echinata, placing them in a comparative evolutionary framework with other cnidarian genomes. We also generated and annotated a single-cell transcriptomic atlas for adult male H. symbiolongicarpus and identified cell type markers for all major cell types, including key i-cell markers. Orthology analyses based on the markers revealed that Hydractinia's i-cells are highly enriched in genes that are widely shared amongst animals, a striking finding given that Hydractinia has a higher proportion of phylum-specific genes than any of the other 41 animals in our orthology analysis. These results indicate that Hydractinia's stem cells and early progenitor cells may use a toolkit shared with all animals, making it a promising model organism for future exploration of stem cell biology and regenerative medicine. The genomic and transcriptomic resources for Hydractinia presented here will enable further studies of their regenerative capacity, colonial morphology, and ability to distinguish self from non-self.more » « less
-
more » « less
Hydractinia is a colonial marine hydroid that shows remarkable biological properties, including the capacity to regenerate its entire body throughout its lifetime, a process made possible by its adult migratory stem cells, known as i-cells. Here, we provide an in-depth characterization of the genomic structure and gene content of twoHydractinia species,Hydractinia symbiolongicarpus andHydractinia echinata , placing them in a comparative evolutionary framework with other cnidarian genomes. We also generated and annotated a single-cell transcriptomic atlas for adult maleH. symbiolongicarpus and identified cell-type markers for all major cell types, including key i-cell markers. Orthology analyses based on the markers revealed thatHydractinia ’s i-cells are highly enriched in genes that are widely shared amongst animals, a striking finding given thatHydractinia has a higher proportion of phylum-specific genes than any of the other 41 animals in our orthology analysis. These results indicate thatHydractinia ’s stem cells and early progenitor cells may use a toolkit shared with all animals, making it a promising model organism for future exploration of stem cell biology and regenerative medicine. The genomic and transcriptomic resources forHydractinia presented here will enable further studies of their regenerative capacity, colonial morphology, and ability to distinguish self from nonself. -
Vieira, Cristina (Ed.)Abstract Genome assemblies are growing at an exponential rate and have proved indispensable for studying evolution but the effort has been biased toward vertebrates and arthropods with a particular focus on insects. Onychophora or velvet worms are an ancient group of cryptic, soil dwelling worms noted for their unique mode of prey capture, biogeographic patterns, and diversity of reproductive strategies. They constitute a poorly understood phylum of exclusively terrestrial animals that is sister group to arthropods. Due to this phylogenetic position, they are crucial in understanding the origin of the largest phylum of animals. Despite their significance, there is a paucity of genomic resources for the phylum with only one highly fragmented and incomplete genome publicly available. Initial attempts at sequencing an onychophoran genome proved difficult due to its large genome size and high repeat content. However, leveraging recent advances in long-read sequencing technology, we present here the first annotated draft genome for the phylum. With a total size of 5.6Gb, the gigantism of the Epiperipatus broadwayi genome arises from having high repeat content, intron size inflation, and extensive gene family expansion. Additionally, we report a previously unknown diversity of onychophoran hemocyanins that suggests the diversification of copper-mediated oxygen carriers occurred independently in Onychophora after its split from Arthropoda, parallel to the independent diversification of hemocyanins in each of the main arthropod lineages.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1007/s00441-021-03459-y
