Bryozoans Research Articles

A new transcriptome resource for Cellaria immersa (Phylum: Bryozoa) reveals candidate genes and proteins related to biomineralization

One of the most salient features of marine bryozoans is their well-calcified skeleton, and many species in this phylum are important reef-builders. To date, the molecular machinery responsible for skeletal formation in these key animals remains unknown. In this study we performed de novo transcriptome assembly from RNA from Cellaria immersa colonies collected in New Zealand, the first from the family Cellariidae. The assembly resulted in a set of 125,750 transcripts and was estimated to be 97.2% complete when compared to BUSCO core gene sets. A function was predicted for 61,442 (48.8%) of the translated proteins, using similarity searches against a range of databases using BLAST and InterProScan. Cellaria species form erect, heavily calcified arborescent colonies, which when abundant can create micro-forests or meadows on the ocean floor. RNA was extracted separately from younger distal and older proximal parts of the colonies, aiming to identify the key genes involved in biomineralization as the young zooids (at the distal growth margin) of the colony are more likely to be actively growing and calcifying compared to the old zooids of the proximal parts of the colony. Differential expression analysis was carried out to identify differential expression between the distal and proximal parts of the colonies. This showed that 506 (2.2%) of the transcripts were expressed more highly in the young zooids and 4,676 (20.4%) were expressed more highly in the old zooids. Over 50 protein families were identified as candidates involved in biomineralization in C. immersa based on the functional annotation, their expression pattern and literature. Transcripts encoding 24 such protein families were more highly expressed in the young zooids. This is the first such study on a heavily calcified species from the phylum Bryozoa, increasing the amount of ‘omics’ data available for C. immersa and the phylum. These data provide a resource for current and future studies of heavily calcified bryozoans, shedding a light on the biomineralization process in this phylum.

Rediscovering the unusual, solitary bryozoan Monobryozoon ambulans Remane, 1936: first molecular and new morphological data clarify its phylogenetic position

BackgroundOne of the most peculiar groups of the mostly colonial phylum Bryozoa is the taxon Monobryozoon, whose name already implies non-colonial members of the phylum. Its peculiarity and highly unusual lifestyle as a meiobenthic clade living on sand grains has fascinated many biologists. In particular its systematic relationship to other bryozoans remains a mystery. Despite numerous searches for M. ambulans in its type locality Helgoland, a locality with a long-lasting marine station and tradition of numerous courses and workshops, it has never been reencountered until today. Here we report the first observations of this almost mythical species, Monobryozoon ambulans.ResultsFor the first time since 1938, we present new modern, morphological analyses of this species as well as the first ever molecular data. Our detailed morphological analysis confirms most previous descriptions, but also ascertains the presence of special ambulatory polymorphic zooids. We consider these as bud anlagen that ultimately consecutively separate from the animal rendering it pseudo-colonial. The remaining morphological data show strong ties to alcyonidioidean ctenostome bryozoans. Our morphological data is in accordance with the phylogenomic analysis, which clusters it with species of Alcyonidium as a sister group to multiporate ctenostomes. Divergence time estimation and ancestral state reconstruction recover the solitary state of M. ambulans as a derived character that probably evolved in the Late Cretaceous. In this study, we also provide the entire mitogenome of M. ambulans, which—despite the momentary lack of comparable data—provides important data of a unique and rare species for comparative aspects in the future.ConclusionsWe were able to provide first sequence data and modern morphological data for the unique bryozoan, M. ambulans, which are both supporting an alcyonidioidean relationship within ctenostome bryozoans.

Anti-Inflammatory Effects of Bioactive Compounds from Seaweeds, Bryozoans, Jellyfish, Shellfish and Peanut Worms.

Inflammation is a defense mechanism of the body in response to harmful stimuli such as pathogens, damaged cells, toxic compounds or radiation. However, chronic inflammation plays an important role in the pathogenesis of a variety of diseases. Multiple anti-inflammatory drugs are currently available for the treatment of inflammation, but all exhibit less efficacy. This drives the search for new anti-inflammatory compounds focusing on natural resources. Marine organisms produce a broad spectrum of bioactive compounds with anti-inflammatory activities. Several are considered as lead compounds for development into drugs. Anti-inflammatory compounds have been extracted from algae, corals, seaweeds and other marine organisms. We previously reviewed anti-inflammatory compounds, as well as crude extracts isolated from echinoderms such as sea cucumbers, sea urchins and starfish. In the present review, we evaluate the anti-inflammatory effects of compounds from other marine organisms, including macroalgae (seaweeds), marine angiosperms (seagrasses), medusozoa (jellyfish), bryozoans (moss animals), mollusks (shellfish) and peanut worms. We also present a review of the molecular mechanisms of the anti-inflammatory activity of these compounds. Our objective in this review is to provide an overview of the current state of research on anti-inflammatory compounds from marine sources and the prospects for their translation into novel anti-inflammatory drugs.

Late CambrianPywackiais a cnidarian, not a bryozoan: Insights from skeletal microstructure

AbstractThe phylum Bryozoa had long been the only major phylum unknown from the Cambrian and by inference the Cambrian Explosion of biodiversity. When described in 2010 as a late Cambrian cryptostome bryozoan,Pywackia baileyiLanding in Landing et al., 2010 became the oldest known bryozoan (early Cambrian bryozoans have since been described). Controversy remains about the phylum-level identification ofPywackiaLanding in Landing et al., 2010—one study proposed an interpretation ofPywackiaas an octocoral. No previous studies of the skeletal microstructure ofPywackiahave employed the analysis of petrographic thin sections and high-magnification scanning electron microscopy. These two methods, with the addition of data from previous studies, are employed in this analysis of skeletal microstructure, a feature often important for higher-level taxonomic identification. Although many candidate groups were considered,Pywackia's distinctive pillar and laminae, porous skeleton like many Cnidaria, topology of the body walls, and growth of modules are consistent with a cnidarian affinity.Pywackiaskeletons with primary microstructure were 100% phosphate mineral and were collected from a setting of pervasive phosphatic replacement, which leaves uncertainty as to the original skeletal composition.Pywackiais not assigned here to a cnidarian class and likely represents an early, rare, short-lived cnidarian evolutionary group.

Protomelission is an early dasyclad alga and not a Cambrian bryozoan.

The animal phyla and their associated body plans originate from a singular burst of evolution occurring during the Cambrian period, over 500 million years ago1. The phylum Bryozoa, the colonial 'moss animals', have been the exception: convincing skeletons of this biomineralizing clade have been absent from Cambrian strata, in part because potential bryozoan fossils are difficult to distinguish from the modular skeletons of other animal and algal groups2,3. At present, the strongest candidate4 is the phosphatic microfossil Protomelission5. Here we describe exceptionally preserved non-mineralized anatomy in Protomelission-like macrofossils from the Xiaoshiba Lagerstätte6. Taken alongside the detailed skeletal construction and the potential taphonomic origin of 'zooid apertures', we consider that Protomelission is better interpreted as the earliest dasycladalean green alga-emphasizing the ecological role of benthic photosynthesizers in early Cambrian communities. Under this interpretation, Protomelission cannot inform the origins of the bryozoan body plan; despite a growing number of promising candidates7-9, there remain no unequivocal bryozoans of Cambrian age.

Microstructure and Crystallographic Characteristics of Stenolaemate Bryozoans (Phylum Bryozoa and Class Stenolaemata)

The bryozoan Cass Stenolaemata is currently represented by the Order Cyclostomata. They produce skeletons made exclusively of calcite crystals assembled into different microstructures. Despite extensive previous research, no appropriate crystallographic techniques have been applied to decipher their crystallographic organization. We present an in-depth crystallographic study of the microstructures of three extant species (Fasciculipora ramosa, Hornera robusta, and Cinctipora elegans) using scanning electron microscopy and associated techniques (energy-dispersive spectroscopy and electron backscatter diffraction), together with atomic force microscopy and micro-computed tomography. We differentiate two microstructures, foliated and tabular calcite, and establish consistent models of their crystallography. Foliated calcite of F. ramosa and C. elegans consists of co-oriented laths arranged with their c-axes parallel to their elongation axis and to their main surfaces, and one a*-axis perpendicular to the latter (sheet texture). Tabular calcite of H. robusta consists of polygonal tablets with the c-axis as fiber axis (axial texture), perpendicular to the tablet surface. The foliated calcite of bryozoans is homeomorph to that of bivalves but has a significantly different crystallography. The tabular calcite of bryozoans lacks the spiral morphology of the tablet-shaped calcite of craniiformis brachiopods and has a different orientation of the c-axis with respect to the constituent tablets.

Unprecedented frequency of mitochondrial introns in colonial bilaterians

Animal mitogenomes are typically devoid of introns. Here, we report the largest number of mitochondrial introns ever recorded from bilaterian animals. Mitochondrial introns were identified for the first time from the phylum Bryozoa. They were found in four species from three families (Order Cheilostomatida). A total of eight introns were found in the complete mitogenome of Exechonella vieirai, and five, 17 and 18 introns were found in the partial mitogenomes of Parantropora penelope, Discoporella cookae and Cupuladria biporosa, respectively. Intron-encoded protein domains reverse transcriptase and intron maturase (RVT-IM) were identified in all species. Introns in E. vieirai and P. penelope had conserved Group II intron ribozyme domains V and VI. Conserved domains were lacking from introns in D. cookae and C. biporosa, preventing their further categorization. Putative origins of metazoan introns were explored in a phylogenetic context, using an up-to-date alignment of mitochondrial RVT-IM domains. Results confirmed previous findings of multiple origins of annelid, placozoan and sponge RVT-IM domains and provided evidence for common intron donor sources across metazoan phyla. Our results corroborate growing evidence that some metazoans with regenerative abilities (i.e. placozoans, sponges, annelids and bryozoans) are susceptible to intron integration, most likely via horizontal gene transfer.

Fossil evidence unveils an early Cambrian origin for Bryozoa

Bryozoans (also known as ectoprocts or moss animals) are aquatic, dominantly sessile, filter-feeding lophophorates that construct an organic or calcareous modular colonial (clonal) exoskeleton1–3. The presence of six major orders of bryozoans with advanced polymorphisms in lower Ordovician rocks strongly suggests a Cambrian origin for the largest and most diverse lophophorate phylum2,4–8. However, a lack of convincing bryozoan fossils from the Cambrian period has hampered resolution of the true origins and character assembly of the earliest members of the group. Here we interpret the millimetric, erect, bilaminate, secondarily phosphatized fossil Protomelission gatehousei9 from the early Cambrian of Australia and South China as a potential stem-group bryozoan. The monomorphic zooid capsules, modular construction, organic composition and simple linear budding growth geometry represent a mixture of organic Gymnolaemata and biomineralized Stenolaemata character traits, with phylogenetic analyses identifying P. gatehousei as a stem-group bryozoan. This aligns the origin of phylum Bryozoa with all other skeletonized phyla in Cambrian Age 3, pushing back its first occurrence by approximately 35 million years. It also reconciles the fossil record with molecular clock estimations of an early Cambrian origination and subsequent Ordovician radiation of Bryozoa following the acquisition of a carbonate skeleton10–13.

Three in one: evolution of viviparity, coenocytic placenta and polyembryony in cyclostome bryozoans

BackgroundPlacentation has evolved multiple times among both chordates and invertebrates. Although they are structurally less complex, invertebrate placentae are much more diverse in their origin, development and position. Aquatic colonial suspension-feeders from the phylum Bryozoa acquired placental analogues multiple times, representing an outstanding example of their structural diversity and evolution. Among them, the clade Cyclostomata is the only one in which placentation is associated with viviparity and polyembryony—a unique combination not present in any other invertebrate group.ResultsThe histological and ultrastructural study of the sexual polymorphic zooids (gonozooids) in two cyclostome species, Crisia eburnea and Crisiella producta, revealed embryos embedded in a placental analogue (nutritive tissue) with a unique structure—comprising coenocytes and solitary cells—previously unknown in animals. Coenocytes originate via nuclear multiplication and cytoplasmic growth among the cells surrounding the early embryo. This process also affects cells of the membranous sac, which initially serves as a hydrostatic system but later becomes main part of the placenta. The nutritive tissue is both highly dynamic, permanently rearranging its structure, and highly integrated with its coenocytic ‘elements’ being interconnected via cytoplasmic bridges and various cell contacts. This tissue shows evidence of both nutrient synthesis and transport (bidirectional transcytosis), supporting the enclosed multiple progeny. Growing primary embryo produces secondary embryos (via fission) that develop into larvae; both the secondary embyos and larvae show signs of endocytosis. Interzooidal communication pores are occupied by 1‒2 specialized pore-cells probably involved in the transport of nutrients between zooids.ConclusionsCyclostome nutritive tissue is currently the only known example of a coenocytic placental analogue, although syncytial ‘elements’ could potentially be formed in them too. Structurally and functionally (but not developmentally) the nutritive tissue can be compared with the syncytial placental analogues of certain invertebrates and chordates. Evolution of the cyclostome placenta, involving transformation of the hydrostatic apparatus (membranous sac) and change of its function to embryonic nourishment, is an example of exaptation that is rather widespread among matrotrophic bryozoans. We speculate that the acquisition of a highly advanced placenta providing massive nourishment might support the evolution of polyembryony in cyclostomes. In turn, massive and continuous embryonic production led to the evolution of enlarged incubating polymorphic gonozooids hosting multiple progeny.

Developmental Process of a Heterozooid: Avicularium Formation in a Bryozoan, Bugulina californica.

In bryozoans (phylum Bryozoa), representative colonial animals mostly found in marine environments, some species possess different types of individuals (heterozooids) specialized in different functions such as defense or structural support for their colonies. Among them, the best-known heterozooids are the avicularia, known to function as defenders. The differentiation processes of heterozooids, including avicularia, should be important keys to understand the evolutionary significance of bryozoans. However, the developmental process of avicularium formation remains to be fully understood. In this study, therefore, in order to understand the detailed developmental process and timing of avicularium formation, extensive observations were carried out in a bryozoan species, Bugulina californica (Cheilostomata, Bugulidae), that possesses adventitious avicularia, by performing stereomicroscopy on live materials, in addition to scanning electron microscopy and histological observations. The whole process can be divided into seven stages based on developmental events. Especially notably, at the earlier stages, there are three major budding events that produce proliferating cell masses corresponding to primordial tissues: (1) budding of the peduncle cushion at the outer margin of the distal part of a young autozooid, (2) budding of the head-part primordium from the peduncle cushion, and (3) budding of the polypide inside the head part. Experimental control of temperature showed that 20°C would be the best to maintain B. californica colonies.

First evidence of virus-like particles in the bacterial symbionts of Bryozoa

Bacteriophage communities associated with humans and vertebrate animals have been extensively studied, but the data on phages living in invertebrates remain scarce. In fact, they have never been reported for most animal phyla. Our ultrastructural study showed for the first time a variety of virus-like particles (VLPs) and supposed virus-related structures inside symbiotic bacteria in two marine species from the phylum Bryozoa, the cheilostomes Bugula neritina and Paralicornia sinuosa. We also documented the effect of VLPs on bacterial hosts: we explain different bacterial ‘ultrastructural types’ detected in bryozoan tissues as stages in the gradual destruction of prokaryotic cells caused by viral multiplication during the lytic cycle. We speculate that viruses destroying bacteria regulate symbiont numbers in the bryozoan hosts, a phenomenon known in some insects. We develop two hypotheses explaining exo- and endogenous circulation of the viruses during the life-cycle of B. neritina. Finally, we compare unusual ‘sea-urchin’-like structures found in the collapsed bacteria in P. sinuosa with so-called metamorphosis associated contractile structures (MACs) formed in the cells of the marine bacterium Pseudoalteromonas luteoviolacea which are known to trigger larval metamorphosis in a polychaete worm.

Draft genome of Bugula neritina, a colonial animal packing powerful symbionts and potential medicines

Many animal phyla have no representatives within the catalog of whole metazoan genome sequences. This dataset fills in one gap in the genome knowledge of animal phyla with a draft genome of Bugula neritina (phylum Bryozoa). Interest in this species spans ecology and biomedical sciences because B. neritina is the natural source of bioactive compounds called bryostatins. Here we present a draft assembly of the B. neritina genome obtained from PacBio and Illumina HiSeq data, as well as genes and proteins predicted de novo and verified using transcriptome data, along with the functional annotation. These sequences will permit a better understanding of host-symbiont interactions at the genomic level, and also contribute additional phylogenomic markers to evaluate Lophophorate or Lophotrochozoa phylogenetic relationships. The effort also fits well with plans to ultimately sequence all orders of the Metazoa.

Trophic habits of the invasive crab Libinia dubia H. Milne Edwards, 1834 from the Gulf of Gabès (Tunisia)

Feeding habits of the invasive spider crab Libinia dubia from the Mediterranean Sea were studied in the Gulf of Gabès (Tunisia) using the frequency of occurrence and points methods. The population was sampled at least monthly between November 2015 and October 2016. Stomach contents of 384 specimens were analysed. Results indicate that L. dubia is an herbivorous species exhibiting clear preferences for algae (ALG) and Magnoliophyta (MAG) (62.03%, 7.13 points and 59.36%, 5.3 points respectively) although Echinodermata (ECH), Porifera (POR), Cnidaria (CNI), Mollusca (MOL), Polychaeta (POL), Crustacea (CRU) and fish (FIS) were accidentally consumed along with Bryozoa (BRY), sediment (SED), and unidentifiable materials (UNM). The diversity of ALG ingested was studied in detail: Chlorophyceae were found in 87.93% of stomachs containing ALG and contributed most of points to the stomach contents (4.18 points) followed respectively by Phaeophyceae (81.03%, 2.27 points) and Rhodophyceae (40.95%, 0.68 points).Very low Vacuity Index was recorded (VI = 2.6%). Ingested items varied significantly with regard to the season (Chi-square test, χ2calculated = 87.86 > χ2theoretical = 7.81, df = 3, p < 0.05) and crab size (χ2calculated = 14.25 > χ2theoretical = 5.99, df = 2, p = 0.026). Insignificant differences were registered by studying Carapace Width-Stomach Weight (CW-SW) relationships (T-test, tcalculated < ttheoretical, p > 0.05). Kruskal-Wallis test was applied so that the composition of crab diet among groups could be compared (H = 1.1, df = 3, p = 0.77).

First transcriptome analysis of bryozoan Fredericella sultana, the primary host of myxozoan parasite Tetracapsuloides bryosalmonae.

Bryozoans are aquatic invertebrate moss animals that are found worldwide. Fredericella sultana is a freshwater bryozoan and is the most common primary host of myxozoan parasite, Tetracapsuloides bryosalmonae. However, limited genomic resources are available for this bryozoan, which hampers investigations into the molecular mechanisms of host-parasite interactions. To better understand these interactions, there is a need to build a transcriptome dataset of F. sultana, for functional genomics analysis by large-scale RNA sequencing. Total RNA was extracted from zooids of F. sultana cultivated under controlled laboratory conditions. cDNA libraries were prepared and were analyzed by the Illumina paired-ends sequencing. The sequencing data were used for de novo transcriptome assembly and functional annotation. Approximately 118 million clean reads were obtained, and assembled into 85,544 contigs with an average length of 852 bp, an N50 of 1,085 bp, and an average GC content 51.4%. A total of 23,978 (28%) contigs were annotated using BLASTX analysis. Of these transcripts, 4,400 contigs had highest similarity to brachiopod species Lingula anatina. Based on Gene ontology (GO) annotation, the most highly scored categories of biological process were categorized into cellular process (27%), metabolic process (24%), and biological regulation (8%) in the transcriptome of F. sultana. This study gives first insights into the transcriptome of F. sultana and provides comprehensive genetic resources for the species. We believe that the transcriptome of F. sultana will serve as a useful genomic dataset to accelerate research of functional genomics and will help facilitate whole genome sequencing and annotation. Candidate genes potentially involved in growth, proteolysis, and stress/immunity-response were identified, and are worthy of further investigation.

The Phylum Bryozoa: From Biology to Biomedical Potential.

Less than one percent of marine natural products characterized since 1963 have been obtained from the phylum Bryozoa which, therefore, still represents a huge reservoir for the discovery of bioactive metabolites with its ~6000 described species. The current review is designed to highlight how bryozoans use sophisticated chemical defenses against their numerous predators and competitors, and which can be harbored for medicinal uses. This review collates all currently available chemoecological data about bryozoans and lists potential applications/benefits for human health. The core of the current review relates to the potential of bryozoan metabolites in human diseases with particular attention to viral, brain, and parasitic diseases. It additionally weighs the pros and cons of total syntheses of some bryozoan metabolites versus the synthesis of non-natural analogues, and explores the hopes put into the development of biotechnological approaches to provide sustainable amounts of bryozoan metabolites without harming the natural environment.

Key novelties in the evolution of the aquatic colonial phylum Bryozoa: evidence from soft body morphology.

ABSTRACTMolecular techniques are currently the leading tools for reconstructing phylogenetic relationships, but our understanding of ancestral, plesiomorphic and apomorphic characters requires the study of the morphology of extant forms for testing these phylogenies and for reconstructing character evolution. This review highlights the potential of soft body morphology for inferring the evolution and phylogeny of the lophotrochozoan phylum Bryozoa. This colonial taxon comprises aquatic coelomate filter‐feeders that dominate many benthic communities, both marine and freshwater. Despite having a similar bauplan, bryozoans are morphologically highly diverse and are represented by three major taxa: Phylactolaemata, Stenolaemata and Gymnolaemata. Recent molecular studies resulted in a comprehensive phylogenetic tree with the Phylactolaemata sister to the remaining two taxa, and Stenolaemata (Cyclostomata) sister to Gymnolaemata. We plotted data of soft tissue morphology onto this phylogeny in order to gain further insights into the origin of morphological novelties and character evolution in the phylum. All three larger clades have morphological apomorphies assignable to the latest molecular phylogeny. Stenolaemata (Cyclostomata) and Gymnolaemata were united as monophyletic Myolaemata because of the apomorphic myoepithelial and triradiate pharynx. One of the main evolutionary changes in bryozoans is a change from a body wall with two well‐developed muscular layers and numerous retractor muscles in Phylactolaemata to a body wall with few specialized muscles and few retractors in the remaining bryozoans. Such a shift probably pre‐dated a body wall calcification that evolved independently at least twice in Bryozoa and resulted in the evolution of various hydrostatic mechanisms for polypide protrusion. In Cyclostomata, body wall calcification was accompanied by a unique detachment of the peritoneum from the epidermis to form the hydrostatic membraneous sac. The digestive tract of the Myolaemata differs from the phylactolaemate condition by a distinct ciliated pylorus not present in phylactolaemates. All bryozoans have a mesodermal funiculus, which is duplicated in Gymnolaemata. A colonial system of integration (CSI) of additional, sometimes branching, funicular cords connecting neighbouring zooids via pores with pore‐cell complexes evolved at least twice in Gymnolaemata. The nervous system in all bryozoans is subepithelial and concentrated at the lophophoral base and the tentacles. Tentacular nerves emerge intertentacularly in Phylactolaemata whereas they partially emanate directly from the cerebral ganglion or the circum‐oral nerve ring in myolaemates. Overall, morphological evidence shows that ancestral forms were small, colonial coelomates with a muscular body wall and a U‐shaped gut with ciliary tentacle crown, and were capable of asexual budding. Coloniality resulted in many novelties including the origin of zooidal polymorphism, an apomorphic landmark trait of the Myolaemata.

The Phylum Bryozoa as a Promising Source of Anticancer Drugs.

Recent advances in sampling and novel techniques in drug synthesis and isolation have promoted the discovery of anticancer agents from marine organisms to combat this major threat to public health worldwide. Bryozoans, which are filter-feeding, aquatic invertebrates often characterized by a calcified skeleton, are an excellent source of pharmacologically interesting compounds including well-known chemical classes such as alkaloids and polyketides. This review covers the literature for secondary metabolites isolated from marine cheilostome and ctenostome bryozoans that have shown potential as cancer drugs. Moreover, we highlight examples such as bryostatins, the most known class of marine-derived compounds from this animal phylum, which are advancing through anticancer clinical trials due to their low toxicity and antineoplastic activity. The bryozoan antitumor compounds discovered until now show a wide range of chemical diversity and biological activities. Therefore, more research focusing on the isolation of secondary metabolites with potential anticancer properties from bryozoans and other overlooked taxa covering wider geographic areas is needed for an efficient bioprospecting of natural products.

The last phylum: Occupation of Bryozoa morpho-ecospace (colony growth habits) during the early phase of the Great Ordovician Biodiversification Event

Most major phyla, and all skeletonized phyla have their first appearance in the Cambrian. The exception is the Phylum Bryozoa, which first appear in the Early Ordovician (Tremadocian 1b). Bryozoans have an excellent fossil record, due in part to their benthic marine habitat with skeletal colonies composed largely of stable, low-Magnesium calcite. These factors provide an unrivaled opportunity to observe patterns and rates of radiation of a new phylum into disparate morpho- ecospace through the Great Ordovician Biodiversification Event (GOBE).In this study, the colonial growth habits of all known skeletonized Bryozoa (181 species) from the Early and Middle Ordovician are characterized in a new classification scheme based on processes of growth, rather than their end geometry as most traditional classifications of bryozoan growth habits. These fundamental categories are: orientation, dimensions of primary growth, width of colony unit, layers of zooecia, substrate relationships, space utilization, skeleton mineralization, plus sub-categories of orientation based on their geometry.In the Early and Middle Ordovician there are 85 unique growth habits defined by these eight growth habit characters. By the end of Middle Ordovician, about 4.8% of the morpho-ecospace defined by two subsets of the characters had been occupied by five bryozoan orders (represented by 34 families, 77 genera). When plotted by Ordovician stage time-slices (ca. 2.2 my each), a sharp increase in taxonomic and growth habit occurrence is observed at the Early-Middle Ordovician transition, earlier than in other groups. Individual growth habit character states also show significant changes at this transition. In the Early Ordovician, low bryozoan taxonomic and growth habit richness is due in part to sampling bias and modified search methods are need, however, the overall patterns (Early-Mid. Ordovician transition) observed in this study are robust and not expected to change fundamentally with additional data.

Seigo Shima

Angewandte Chemie International EditionVolume 58, Issue 24 p. 7910-7910 Author ProfileFree Access Seigo Shima First published: 17 January 2019 https://doi.org/10.1002/anie.201900274AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinkedInRedditWechat Graphical Abstract “I am waiting for the day when someone will discover a method to predict earthquakes. If I could be described as an animal it would be a mouse …” Find out more about Seigo Shima in his Author Profile. Seigo Shima The author presented on this page has published more than 10 articles in Angewandte Chemie in the last 10 years, most recently: “The bacterial [Fe]-hydrogenase paralog HmdII uses tetrahydrofolate derivatives as substrates”: T. Watanabe, T. Wagner, G. Huang, J. Kahnt, K. Ataka, U. Ermler, S. Shima, Angew. Chem. Int. Ed. 2019, DOI: 10.1002/anie.201813465; Angew. Chem. 2019, DOI: 10.1002/ange.201813465. The work of S. Shima has been featured as a frontispiece communication in Angewandte Chemie: “Crystal Structures of [Fe]-Hydrogenase in Complex with Inhibitory Isocyanides: Implications for the H2-Activation Site”: H. Tamura, M. Salomone-Stagni, T. Fujishiro, E. Warkentin, W. Meyer-Klaucke, U. Ermler, S. Shima, Angew. Chem. Int. Ed. 2013, 52, 9656; Angew. Chem. 2013, 125, 9838. Date of birth: November 5, 1960 Position: Research Group Leader at the Max Planck Institute for Terrestrial Microbiology, Guest Professor at The Institute of Low Temperature Science at Hokkaido University E-mail: shima@mpi-marburg.mpg.de Homepage: https://www.mpi-marburg.mpg.de/shima ORCID: org/0000-0003-1872-8705 Education: 1985 Master, Osaka Prefectural University 1991 Ph.D., Prof. Tohru Kodama, University of Tokyo 1993–1995 Alexander von Humboldt Research Fellow, Prof. Rudolf K. Thauer, Philipps Universität Marburg Awards: 2013 JSPS Alumni Club Award, 2013 The conversion of light energy prize from a PRESTO program of Japan Science and Technology Agency Research: Catalytic mechanisms of metalloenzymes, biosynthesis of metallocofactors Hobbies: Do-it-yourself, walking, listening to music My motto is “relax and enjoy”. When I was eighteen I wanted to be a microbiologist. If I could be described as an animal it would be a mouse. I am waiting for the day when someone will discover a method to predict earthquakes. The biggest challenge facing scientists is climate change. Science is fun because we can directly learn from nature. My favorite drink is Port Wine. My first experiment was bacterial-colony counting. My favorite time of day is walking in the forest to the institute. My favorite way to spend a holiday is to visit restaurants in foreign towns. My favorite name of molecule is the FeGP cofactor. If I could be a piece of lab equipment, I would be a balance. My favorite painter is Günter Blau. My favorite composer is Johann Sebastian Bach. My 5 top papers: 1“A conspicuous nickel protein in microbial mats that oxidize methane anaerobically”: M. Krüger, A. Meyerdierks, F. O. Glöckner, R. Amann, F. Widdel, M. Kube, R. Reinhardt, J. Kahnt, R. Böcher, R. K. Thauer, S. Shima, Nature 2003, 426, 878. We isolated and characterized nickel enzymes that catalyze the anaerobic oxidation of methane. 2“The Crystal Structure of [Fe]-Hydrogenase Reveals the Geometry of the Active Site ”: S. Shima, O. Pilak, S. Vogt, M. Schick, M. S. Stagni, W. Meyer-Klaucke, E. Warkentin, R. K. Thauer, U. Ermler, Science 2008, 321, 572. We proposed a model of the iron center of [Fe]-hydrogenase. 3“Structure of a methyl-coenzyme M reductase from Black Sea mats that oxidize methane anaerobically”: S. Shima, M. Krueger, T. Weinert, U. Demmer, J. Kahnt, R. K. Thauer, U. Ermler, Nature 2012, 481, 98. We crystallized a methane-oxidizing enzyme from a protein mixture prepared from the natural microbial mat. 4“The methanogenic CO2 reducing-and-fixing enzyme is bifunctional and contains 46 [4Fe-4S] clusters”: T. Wagner, U. Ermler, S. Shima, Science 2016, 354, 114. We found very long electron wires made of iron-sulfur clusters, which connect the four tungsten-containing active sites. 5“Methanogenic heterodisulfide reductase (HdrABC-MvhAGD) uses two noncubane [4Fe-4S] clusters for reduction”: T. Wagner, J. Koch, U. Ermler, S. Shima, Science 2017, 357, 699. We found a new type of iron-sulfur cluster. Volume58, Issue24June 11, 2019Pages 7910-7910 ReferencesRelatedInformation

Lower Oligocene Coralline Algae of the Uromieh Section (Qom Formation, NW Iran) and the oldest record of Titanoderma pustulatum (Corallinophycidae, Rhodophyta)

The Rupelian Uromieh section of the Qom Formation was analyzed with the aim to provide a first description of its coralline algal assemblages, and benthic paleoenvironmental evolution through time. The presence of Nummulites fichteli , Nummulites vascus , Halkyardia maxima and Subterraniphyllum thomasii , together with the absence of Nephrolepidina and Eulepidina confirm an early to middle Rupelian age. In the lower part of the section, the abundance of miliolids and corals suggests a proximal inner-platform environment, while upsection the increase in large rotaliids, coralline algae and bryozoans points toward a distal inner-platform/proximal middle-platform setting. Coralline algal assemblages support this interpretation, with Sporolithales and Hapalidiales becoming more common in the upper part of the section. Within the coralline assemblage, Lithoporella melobesioides and Titanoderma pustulatum are two of the most common species, together with articulated coralline algae. S. thomasii is more common in coral-rich intervals, confirming that the distribution of this species was confined to shallow-water environments. The specimens of T. pustulatum recovered in the Uromieh section predate all the other known records of this species, indicating that the origin of T. pustulatum should be dated at least at the early Rupelian