The ribbon architecture of the Golgi apparatus is not restricted to vertebrates

The Golgi apparatus plays a central role as a processing and sorting station along the secretory pathway. In multicellular organisms, this organelle displays two structural organizations, whereby its functional subunits, the mini-stacks, are either dispersed throughout the cell or linked into a centralized structure, called Golgi “ribbon”. The Golgi ribbon is considered to be a feature typical of vertebrate cells. Here we report that this is not the case. We show that sea urchin embryonic cells assemble Golgi ribbons during early development. Sea urchins are deuterostomes, the bilaterian animal clade to which chordates, and thus vertebrates, also belong.Far from being a structural innovation of vertebrates, the Golgi ribbon therefore appears to be an ancient cellular feature evolved before the split between echinoderms and chordates. Evolutionary conservation of the ribbon architecture surmises that it must play fundamental roles in the biology of deuterostomes.

A cohort of Caenorhabditis species lacking the highly conserved let-7 microRNA

The let-7 gene encodes a highly conserved microRNA with critical functions integral to cell fate specification and developmental progression in diverse animals. In Caenorhabditis elegans, let-7 is a component of the heterochronic (developmental timing) gene regulatory network, and loss-of-function mutations of let-7 result in lethality during the larval to adult transition due to misregulation of the conserved let-7 target, lin-41. To date, no bilaterian animal lacking let-7 has been characterized. In this study, we identify a cohort of nematode species within the genus Caenorhabditis, closely related to C. elegans, that lack the let-7 microRNA, owing to absence of the let-7 gene. Using C. sulstoni as a representative let-7-lacking species to characterize normal larval development in the absence of let-7, we demonstrate that, except for the lack of let-7, the heterochronic gene network is otherwise functionally conserved. We also report that species lacking let-7 contain a group of divergent let-7 paralogs—also known as the let-7-family of microRNAs—that have apparently assumed the role of targeting the lin-41 mRNA.

Unravelling the developmental and functional significance of an ancient Argonaute duplication

MicroRNAs (miRNAs) base-pair to messenger RNA targets and guide Argonaute proteins to mediate their silencing. This target regulation is considered crucial for animal physiology and development. However, this notion is based exclusively on studies in bilaterians, which comprise almost all lab model animals. To fill this phylogenetic gap, we characterize the functions of two Argonaute paralogs in the sea anemone Nematostella vectensis of the phylum Cnidaria, which is separated from bilaterians by ~600 million years. Using genetic manipulations, Argonaute-immunoprecipitations and high-throughput sequencing, we provide experimental evidence for the developmental importance of miRNAs in a non-bilaterian animal. Additionally, we uncover unexpected differential distribution of distinct miRNAs between the two Argonautes and the ability of one of them to load additional types of small RNAs. This enables us to postulate a novel model for evolution of miRNA precursors in sea anemones and their relatives, revealing alternative trajectories for metazoan miRNA evolution.

A cohort of Caenorhabditis species lacking the highly conserved let-7 microRNA

ABSTRACTlet-7 is a highly conserved microRNA with critical functions integral to cell fate specification and developmental progression in diverse animals. In Caenorhabditis elegans, let-7 is a component of the heterochronic (developmental timing) gene regulatory network, and loss-of-function mutations of let-7 result in lethality during the larval to adult transition due to misregulation of the conserved let-7 target, lin-41. To date, no bilaterian animal lacking let-7 has been characterized. In this study, we identify a cohort of nematode species within the genus Caenorhabditis, closely related to C. elegans, that lack the let-7 microRNA, owing to absence of the let-7 gene. Using C. sulstoni as a representative let-7-lacking species to characterize normal larval development in the absence of let-7, we demonstrate that, except for the lack of let-7, the heterochronic gene network is otherwise functionally conserved. We also report that species lacking let-7 contain a group of divergent let-7 orthologs -- also known as the let-7-family of microRNAs -- that have apparently assumed the role of targeting the lin-41 mRNA.Summary StatementWe have identified a group of Caenorhabditis species that lack let-7a, an otherwise highly conserved and nearly ubiquitous microRNA that was previously thought to be critical to bilaterian animal development.

Hedgehog signaling is required for endomesodermal patterning and germ cell development in the sea anemone Nematostella vectensis

Two distinct mechanisms for primordial germ cell (PGC) specification are observed within Bilatera: early determination by maternal factors or late induction by zygotic cues. Here we investigate the molecular basis for PGC specification in Nematostella, a representative pre-bilaterian animal where PGCs arise as paired endomesodermal cell clusters during early development. We first present evidence that the putative PGCs delaminate from the endomesoderm upon feeding, migrate into the gonad primordia, and mature into germ cells. We then show that the PGC clusters arise at the interface between hedgehog1 and patched domains in the developing mesenteries and use gene knockdown, knockout and inhibitor experiments to demonstrate that Hh signaling is required for both PGC specification and general endomesodermal patterning. These results provide evidence that the Nematostella germline is specified by inductive signals rather than maternal factors, and support the existence of zygotically-induced PGCs in the eumetazoan common ancestor.

Unravelling the developmental and functional significance of an ancient Argonaute duplication

AbstractmicroRNAs (miRNAs), base-pair to messenger RNA targets and guide Argonaute proteins to mediate their silencing. This target regulation is considered crucial for animal physiology and development. However, this notion is based exclusively on studies in bilaterians, which comprise almost all lab model animals. To fill this glaring phylogenetic gap, we characterized the functions of two Argonaute paralogs in the sea anemone Nematostella vectensis of the phylum Cnidaria, which is separated from bilaterians by ∼600 million years. Using genetic manipulation, Argonaute-immunoprecipitations and high-throughput sequencing we provide experimental evidence for the developmental importance of miRNAs in a non-bilaterian animal. Additionally, we uncover unexpected differential distribution of distinct miRNAs between the two Argonautes and the ability of one of them to load additional types of small RNAs. This enables us to postulate a novel model for evolution of miRNA precursors in sea anemones and their relatives, revealing alternative trajectories for metazoan miRNA evolution.

Hedgehog signaling is required for endomesodermal patterning and germ cell development in Nematostella vectensis

Two distinct mechanisms for primordial germ cell (PGC) specification are observed within Bilatera: early determination by maternal factors or late induction by zygotic cues. Here we investigate the molecular basis for PGC specification in Nematostella, a representative pre-bilaterian animal where PGCs arise as paired endomesodermal cell clusters during early development. We first present evidence that the putative PGCs delaminate from the endomesoderm upon feeding, migrate into the gonad primordia, and mature into germ cells. We then show that the PGC clusters arise at the interface between hedgehog1 and patched domains in the developing mesenteries and use gene knockdown, knockout and inhibitor experiments to demonstrate that Hh signaling is required for both PGC specification and general endomesodermal patterning. These results provide evidence that the Nematostella germline is specified by inductive signals rather than maternal factors, and support the existence of zygotically-induced PGCs in the eumetazoan common ancestor.

Surfing in and on microbial mats: Oxygen-related behavior of a terminal Ediacaran bilaterian animal

Geochemical evidence suggests that terminal Ediacaran (ca. 551–539 Ma) oceans experienced expansive anoxia and dynamic redox conditions, which are expected to have impacted animal distribution and behaviors. However, fossil evidence for oxygen-related behaviors of terminal Ediacaran animals is poorly documented. Here, we report a terminal Ediacaran trace fossil that records redox-regulated behaviors. This trace fossil, Yichnus levis new ichnogenus and new ichnospecies, consists of short and uniserially aligned segments of horizontal burrows that are closely associated with microbial mats. Thin-section analysis shows that the trace-making animal moved repeatedly in and out of microbial mats, with mat-burrowing intervals interspersed by epibenthic intermissions. This animal is hypothesized to have been a bilaterian exploring an oxygen oasis in microbial mats. Such intermittent burrowing behavior reflects challenging and dynamic redox conditions in both the water column and microbial mats, highlighting the close relationship between terminal Ediacaran animals and redox dynamics.

Sedimentology and chemostratigraphy of the terminal Ediacaran Dengying Formation at the Gaojiashan section, South China

The terminal Ediacaran Dengying Formation (c. 551.1–538.8 Ma) in South China is one of two successions where Ediacara-type macrofossils are preserved in carbonate facies along with skeletal fossils and bilaterian animal traces. Given the remarkable thickness of carbonate-bearing strata deposited in less than 12.3 million years, the Dengying Formation holds the potential for construction of a relatively continuous chemostratigraphic profile for the terminal Ediacaran Period. In this study, a detailed sedimentological and chemostratigraphic (δ13Ccarb, δ18Ocarb, δ13Corg, δ34Spyrite, and 87Sr/86Sr) investigation was conducted on the Dengying Formation at the Gaojiashan section, Ningqiang County of southern Shaanxi Province, South China. Sedimentological results reveal an overall shallow-marine depositional environment. Carbonate breccia, void-filling botryoidal precipitates and aragonite crystal fans are common in the Algal Dolomite Member of the Dengying Formation, suggesting that peritidal facies were repeatedly karstified. The timing of karstification was likely early, probably soon after the deposition of the dolomite sediments. The presence of authigenic aragonite cements suggests high alkalinity in the terminal Ediacaran ocean. Geochemical analysis of micro-drilled samples shows that distinct compositions are registered in different carbonate phases, which should be considered when constructing chemostratigraphic profiles representative of true temporal variations in seawater chemistry. Integrated chemostratigraphic data suggest enhanced burial of organic carbon and pyrite, and the occurrence of extensive marine anoxia (at least in the Gaojiashan Member). Rapid basinal subsidence and carbonate accumulation during a time of elevated seawater alkalinity and increased rates of pyrite burial may have facilitated the evolutionary innovation of early biomineralizing metazoans.

Collagen IV and basement membrane at the evolutionary dawn of metazoan tissues

The role of the cellular microenvironment in enabling metazoan tissue genesis remains obscure. Ctenophora has recently emerged as one of the earliest-branching extant animal phyla, providing a unique opportunity to explore the evolutionary role of the cellular microenvironment in tissue genesis. Here, we characterized the extracellular matrix (ECM), with a focus on collagen IV and its variant, spongin short-chain collagens, of non-bilaterian animal phyla. We identified basement membrane (BM) and collagen IV in Ctenophora, and show that the structural and genomic features of collagen IV are homologous to those of non-bilaterian animal phyla and Bilateria. Yet, ctenophore features are more diverse and distinct, expressing up to twenty genes compared to six in vertebrates. Moreover, collagen IV is absent in unicellular sister-groups. Collectively, we conclude that collagen IV and its variant, spongin, are primordial components of the extracellular microenvironment, and as a component of BM, collagen IV enabled the assembly of a fundamental architectural unit for multicellular tissue genesis.