Metazoan Animals Research Articles

The Shared Origins of Embodiment and Development.

As a domain of study centering on the nature of the body in the functioning of the individual organism, embodiment encompasses a diverse array of topics and questions. One useful organizing framework places embodiment as a bridge construct connecting three standpoints on the body: the form of the body, the body as actively engaged in and with the world, and the body as lived experience. Through connecting these standpoints, the construct of embodiment shows that they are not mutually exclusive: inherent in form is the capacity for engagement, and inherent in engagement is a lived perspective that confers agency and meaning. Here, we employ this framework to underscore the deep connections between embodiment and development. We begin with a discussion of the origins of multicellularity, highlighting how the evolution of bodies was the evolution of development itself. The evolution of the metazoan (animal) body is of particular interest, because most animals possess complex bodies with sensorimotor capacities for perceiving and acting that bring forth a particular sort of embodiment. However, we also emphasize that the thread of embodiment runs through all living things, which share an organizational property of self-determination that endows them with a specific kind of autonomy. This realization moves us away from a Cartesian machine metaphor and instead puts an emphasis on the lived perspective that arises from being embodied. This broad view of embodiment presents opportunities to transcend the boundaries of individual disciplines to create a novel integrative vision for the scientific study of development.

Can Sexual Selection Drive the Evolution of Sperm Cell Structure?

Sperm cells have undergone an extraordinarily divergent evolution among metazoan animals. Parker recognized that because female animals frequently mate with more than one male, sexual selection would continue after mating and impose strong selection on sperm cells to maximize fertilization success. Comparative analyses among species have revealed a general relationship between the strength of selection from sperm competition and the length of sperm cells and their constituent parts. However, comparative analyses cannot address causation. Here, we use experimental evolution to ask whether sexual selection can drive the divergence of sperm cell phenotype, using the dung beetle Onthophagus taurus as a model. We either relaxed sexual selection by enforcing monogamy or allowed sexual selection to continue for 20 generations before sampling males and measuring the total length of sperm cells and their constituent parts, the acrosome, nucleus, and flagella. We found differences in the length of the sperm cell nucleus but no differences in the length of the acrosome, flagella, or total sperm length. Our data suggest that different sperm cell components may respond independently to sexual selection and contribute to the divergent evolution of these extraordinary cells.

Nutrient addition increases rotifer abundance and diversity in a temperate bog

Rotifers are among the smallest metazoan animals living in lakes, ponds, rivers and in interstitial water within Sphagnum mats. When in sufficient numbers they are capable of regenerating large amounts of nitrogen (N) as NO3 and NH4 and phosphorus (P) as PO4; all of these nutrients are immediately available to bog plants. The ecological role of rotifers in bog ecosystems has been recognized at both local and global scales, but the effect of N and P addition on rotifers in bogs remains unknown. Here we present data on the influence of N and P addition on rotifers at a temperate Canadian bog dominated by Sphagnum mosses. We found that rotifer species abundance and diversity were significantly higher in surficial pore water after long-term exposure to increased N and P addition than in the control. A change in plant species distribution and increased rotifer abundance may partly explain the faster decomposition rates, jeopardizing the carbon sink capacity of bogs.

Comparative Biology of Oxygen Sensing in Plants and Animals

Aerobic respiration is essential to almost all eukaryotes and sensing oxygen is a key determinant of survival. Analogous but mechanistically different oxygen-sensing pathways were adopted in plants and metazoan animals, and include ubiquitin-mediated degradation of transcription factors and direct sensing via non-heme iron(Fe2+)-dependent-dioxygenases. Key roles for oxygen sensing have been identified in both groups, with downstream signalling focussed on regulating gene transcription and chromatin modification to control development and stress responses. Components of sensing systems are promising targets for human therapeutic intervention and developing stress-resilient crops. Here, we review current knowledge about the origins, commonalities and differences between oxygen sensing in plants and animals.

Coupled cycling and regulation of metazoan morphogenesis

Metazoan animals are characterized by restricted phenotypic heterogeneity (i.e. morphological disparity) of organisms within various species, a feature that contrasts sharply with intra-species morphological diversity observed in the plant kingdom. Robust emergence of morphogenic blueprint in metazoan animals reflects restricted autonomy of individual cells in adoption of fate outcomes such as differentiation. Fates of individual cells are linked to and influenced by fates of neighboring cells at the population level. Such coupling is a common property of all self-organising systems and propels emergence of order from simple interactions between individual cells without supervision by external directing forces. As a consequence of coupling, expected functional relationship between the constituent cells of an organ system is robustly established concurrent with multiple rounds of cell division during morphogenesis. Notably, the molecular regulation of multicellular coupling during morphogenic self-organisation remains largely unexplored. Here, we review the existing literature on multicellular self-organisation with particular emphasis on recent discovery that β-catenin is the key coupling factor that programs emergence of multi-cellular self-organisation by regulating synchronised cycling of individual cells.

Complete mitochondrial genomes of two deep-sea pandalid shrimps, Heterocarpus ensifer and Bitias brevis: insights into the phylogenetic position of Pandalidae (Decapoda: Caridea)

The mitochondrial genome (mitogenome) analysis is a significant tool for investigating the evolutionary history of metazoan animals. The family Pandalidae is a diverse caridean group containing mainly deep-sea species. Until May 30 2019, only two complete mitogenomes are available in GenBank. Here we present the complete mitogenome sequences of two deep-sea pandalid shrimps, Heterocarpus ensifer and Bitias brevis through Illumina sequencing. The mitochondrial genomes were determined to be 15 939 bp and 15 891 bp long, and both consist of 13 protein-coding genes (PCGs), 23 transfer-RNA genes (tRNAs), two ribosomal-RNA genes (rRNAs), and one control region. The nucleotide composition is biased toward adenine and thymine. Overall, the gene contents and arrangements are consistent with the pancrustacean ground pattern. The alignment of the control regions of four pandalids reveals a conserved sequence block (CSB) (104 bp in length, average GC%=29.47% and 69.23% similarity). A phylogenetic analysis based on 51 Caridea complete mitogenomes revealed that the deep-sea pandalid shrimps are situated an intermediate lineage, with a tendency to originated from those living in shallow sea area.

Genome-wide identification and characterization of heat shock protein family 70 provides insight into its divergent functions on immune response and development of Paralichthys olivaceus.

Flatfish undergo extreme morphological development and settle to a benthic in the adult stage, and are likely to be more susceptible to environmental stress. Heat shock proteins 70 (hsp70) are involved in embryonic development and stress response in metazoan animals. However, the evolutionary history and functions of hsp70 in flatfish are poorly understood. Here, we identified 15 hsp70 genes in the genome of Japanese flounder (Paralichthys olivaceus), a flatfish endemic to northwestern Pacific Ocean. Gene structure and motifs of the Japanese flounder hsp70 were conserved, and there were few structure variants compared to other fish species. We constructed a maximum likelihood tree to understand the evolutionary relationship of the hsp70 genes among surveyed fish. Selection pressure analysis suggested that four genes, hspa4l, hspa9, hspa13, and hyou1, showed signs of positive selection. We then extracted transcriptome data on the Japanese flounder with Edwardsiella tarda to induce stress, and found that hspa9, hspa12b, hspa4l, hspa13, and hyou1 were highly expressed, likely to protect cells from stress. Interestingly, expression patterns of hsp70 genes were divergent in different developmental stages of the Japanese flounder. We found that at least one hsp70 gene was always highly expressed at various stages of embryonic development of the Japanese flounder, thereby indicating that hsp70 genes were constitutively expressed in the Japanese flounder. Our findings provide basic and useful resources to better understand hsp70 genes in flatfish.

Experimental Manipulation of Ploidy in Zebrafish Embryos and Its Application in Genetic Screens.

Metazoan animals are typically diploid, possessing two sets of a chromosome in the somatic cells of an organism. In naturally diploid species, alteration from the endogenous diploid state is usually embryonic lethal. However, the ability to experimentally manipulate ploidy of animal embryos has fundamental as well as applied biology advantages. In this chapter we describe experimental procedures to convert normally diploid zebrafish embryos into haploid or tetraploid states. We also describe methodologies to verify the ploidy of embryos and the utility of ploidy manipulation in expediting the isolation of mutations using both forward and reverse genetic strategies in zebrafish.

Large-Scale Analyses of Site-Specific Evolutionary Rates across Eukaryote Proteomes Reveal Confounding Interactions between Intrinsic Disorder, Secondary Structure, and Functional Domains.

Various structural and functional constraints govern the evolution of protein sequences. As a result, the relative rates of amino acid replacement among sites within a protein can vary significantly. Previous large-scale work on Metazoan (Animal) protein sequence alignments indicated that amino acid replacement rates are partially driven by a complex interaction among three factors: intrinsic disorder propensity; secondary structure; and functional domain involvement. Here, we use sequence-based predictors to evaluate the effects of these factors on site-specific sequence evolutionary rates within four eukaryotic lineages: Metazoans; Plants; Saccharomycete Fungi; and Alveolate Protists. Our results show broad, consistent trends across all four Eukaryote groups. In all four lineages, there is a significant increase in amino acid replacement rates when comparing: (i) disordered vs. ordered sites; (ii) random coil sites vs. sites in secondary structures; and (iii) inter-domain linker sites vs. sites in functional domains. Additionally, within Metazoans, Plants, and Saccharomycetes, there is a strong confounding interaction between intrinsic disorder and secondary structure—alignment sites exhibiting both high disorder propensity and involvement in secondary structures have very low average rates of sequence evolution. Analysis of gene ontology (GO) terms revealed that in all four lineages, a high fraction of sequences containing these conserved, disordered-structured sites are involved in nucleic acid binding. We also observe notable differences in the statistical trends of Alveolates, where intrinsically disordered sites are more variable than in other Eukaryotes and the statistical interactions between disorder and other factors are less pronounced.

How Many Clocks, How Many Times? On the Sensory Basis and Computational Challenges of Circadian Systems.

A vital task for every organism is not only to decide what to do but also when to do it. For this reason, “circadian clocks” have evolved in virtually all forms of life. Conceptually, circadian clocks can be divided into two functional domains; an autonomous oscillator creates a ~24 h self-sustained rhythm and sensory machinery interprets external information to alter the phase of the autonomous oscillation. It is through this simple design that variations in external stimuli (for example, daylight) can alter our sense of time. However, the clock’s simplicity ends with its basic concept. In metazoan animals, multiple external and internal stimuli, from light to temperature and even metabolism have been shown to affect clock time. This raises the fundamental question of cue integration: how are the many, and potentially conflicting, sources of information combined to sense a single time of day? Moreover, individual stimuli, are often detected through various sensory pathways. Some sensory cells, such as insect chordotonal neurons, provide the clock with both temperature and mechanical information. Adding confusion to complexity, there seems to be not only one central clock in the animal’s brain but numerous additional clocks in the body’s periphery. It is currently not clear how (or if) these “peripheral clocks” are synchronized to their central counterparts or if both clocks “tick” independently from one another. In this review article, we would like to leave the comfort zones of conceptual simplicity and assume a more holistic perspective of circadian clock function. Focusing on recent results from Drosophila melanogaster we will discuss some of the sensory, and computational, challenges organisms face when keeping track of time.

Reactivation of RNA metabolism underlies somatic restoration after adult reproductive diapause in C. elegans.

The mechanisms underlying biological aging are becoming recognized as therapeutic targets to delay the onset of multiple age-related morbidities. Even greater health benefits can potentially be achieved by halting or reversing age-associated changes. C. elegans restore their tissues and normal longevity upon exit from prolonged adult reproductive diapause, but the mechanisms underlying this phenomenon remain unknown. Here, we focused on the mechanisms controlling recovery from adult diapause. Here, we show that functional improvement of post-mitotic somatic tissues does not require germline signaling, germline stem cells, or replication of nuclear or mitochondrial DNA. Instead a large expansion of the somatic RNA pool is necessary for restoration of youthful function and longevity. Treating animals with the drug 5-fluoro-2'-deoxyuridine prevents this restoration by blocking reactivation of RNA metabolism. These observations define a critical early step during exit from adult reproductive diapause that is required for somatic rejuvenation of an adult metazoan animal.

The 4D Nucleome: Genome Compartmentalization in an Evolutionary Context.

4D nucleome research aims to understand the impact of nuclear organization in space and time on nuclear functions, such as gene expression patterns, chromatin replication, and the maintenance of genome integrity. In this review we describe evidence that the origin of 4D genome compartmentalization can be traced back to the prokaryotic world. In cell nuclei of animals and plants chromosomes occupy distinct territories, built up from ~1 Mb chromatin domains, which in turn are composed of smaller chromatin subdomains and also form larger chromatin domain clusters. Microscopic evidence for this higher order chromatin landscape was strengthened by chromosome conformation capture studies, in particular Hi-C. This approach demonstrated ~1 Mb sized, topologically associating domains in mammalian cell nuclei separated by boundaries. Mutations, which destroy boundaries, can result in developmental disorders and cancer. Nucleosomes appeared first as tetramers in the Archaea kingdom and later evolved to octamers built up each from two H2A, two H2B, two H3, and two H4 proteins. Notably, nucleosomes were lost during the evolution of the Dinoflagellata phylum. Dinoflagellate chromosomes remain condensed during the entire cell cycle, but their chromosome architecture differs radically from the architecture of other eukaryotes. In summary, the conservation of fundamental features of higher order chromatin arrangements throughout the evolution of metazoan animals suggests the existence of conserved, but still unknown mechanism(s) controlling this architecture. Notwithstanding this conservation, a comparison of metazoans and protists also demonstrates species-specific structural and functional features of nuclear organization.

Wnt gene family members and their expression profiling in Litopenaeus vannamei

The Wnt gene family encodes secreted glycoproteins involved in a wide variety of biological processes, including embryo development, cell proliferation and differentiation, and tissue regeneration. The Wnt pathway exists in all metazoan animals, however, the relevant research is rare in crustaceans. Here we described 12 Wnt genes representing 12 Wnt gene subfamilies in the Pacific white shrimp, Litopenaeus vannamei. Based on homolog annotations and phylogenetic analyses, we named these 12 Wnt genes as LvWnt1, LvWnt2, LvWnt4-11, LvWnt16, and LvWntA. All the corresponding LvWnt proteins shared a conserved Wnt1 domain and 22 conserved cysteine residues. LvWnt1 and LvWnt6 were adjacent in a scaffold in the shrimp genome. Furthermore, we performed expression analyses of LvWnt genes at different developmental stages, during the molting process, in different tissues and after different pathogenic infection. We showed that each LvWnt gene had a unique expression pattern at different developmental stages but only a few of them expressed in adult shrimp. All the investigated LvWnt genes were initially expressed at the gastrula or limb bud embryo stages. Among them, LvWnt8 was specifically high expressed only in early embryos. LvWntA and LvWnt5 displayed high and similar expression profiles during the molting process, and LvWnt6 and LvWnt16 were specifically expressed in the thoracic ganglion, ventral nerve, intestines and gill tissues, respectively. We also found the expression of LvWntA, LvWnt5, LvWnt6, LvWnt9, and LvWnt16 were varied in the different tissues after infected with Staphylococcus aureus, Vibrio parahaemolyticus and white spot syndrome virus (WSSV), which indicated that they might participate in immune response in L. vannamei. This study provided an insight into the repertoire of the Wnt gene structure and expression in shrimps, and furthermore, might promote the understanding of development, growth and immune response of shrimps and crustaceans.

Biological and Pathological Roles of Ganglioside Sialidases.

Sialidases are glycosidases responsible for the removal of α-glycosidically linked sialic acid residues from carbohydrate portions of glycoproteins and glycolipids, this process being the initial step in the degradation of such glycoconjugates. Sialic acids are considered to play important roles in various biological processes largely in two ways, one related to their hydrophilic and acidic properties exerting physicochemical effects on the glycoconjugates to which they are attached, and the other as recognition sites or in an opposing fashion as masking sites. The removal of sialic acids catalyzed by a sialidase, therefore greatly influences many biological processes through changing the conformation of glycoproteins and through recognition and masking of biological sites of functional molecules. Sialidases are found widely distributed in metazoan animals, from echinoderms to mammals, and are also present in viruses and other microorganisms, including fungi, protozoa, and bacteria even mostly lacking sialic acids. In mammals, there are four forms of sialidase (Neu1, Neu2, Neu3, and Neu4), differing in their major subcellular localization and enzymatic properties. They have been implicated in regulation of various cellular activities, such as cell differentiation, cell growth, and cell adhesion and motility, depending on their particular properties. In contrast, in microorganisms the enzymes appear to play roles limited to nutrition and pathogenesis. In this chapter, the focus is on mammalian sialidases preferentially hydrolyzing gangliosides, mostly Neu3 and Neu4, with an attempt to provide a brief overview of their physiological and pathological roles.

Novel and Conserved Features of the Hox Cluster of Entoprocta (Kamptozoa)

Hox genes are highly conserved developmental genes involved in the patterning of the anterior-posterior axis of nearly all metazoan animals. While Hox genes have been characterized for many bilaterians, several cryptic taxa, often comprising microscopic specimens, have hitherto been neglected. We here present the first combined transcriptomic and genomic Hox gene study for Entoprocta (=Kamptozoa), a phylum of microscopic, sessile, tentacle-bearing animals with unresolved phylogenetic affinities. We identified 10 of the 11 Hox genes commonly found in other lophotrochozoans. The analyses of transcriptomic data of different developmental stages of three species (regenerating stages of the colonial species Pedicellina cernua, budding stages of the solitary species Loxosomella vivipara and embryos of the solitary species Loxosomella murmanica/atkinsae) yielded the Hox genes Labial, Hox3, Lox5, and Post2 in all species. Pb and Dfd were only found being expressed in the colonial species P. cernua. Lox4 was uniquely expressed in the solitary species L. vivipara and L. murmanica/atkinsae. Other homeobox genes belonging to the ANTP-class genes, e.g., ParaHox and NK-like genes, were also found. Thus, in addition to newly identified Hox genes (PceLox2-like & LviPost2-like), Entoporocta show the typical lophotrochozoan Hox pattern besides the loss of the posterior class Hox gene Post1.

F-type Lectin Domains: Provenance, Prevalence, Properties, Peculiarities, and Potential.

F-type lectins are phylogenetically widespread albeit selectively distributed lectins with an L-fucose-binding sequence motif and an F-type lectin fold. Several F-type lectins from fishes have been extensively studied, and structural information is available for F-type lectin domains from fish and bacterial proteins. F-type lectins have been demonstrated to be involved in self-/nonself-recognition and therefore have an important role in pathogen defense in many metazoan animals. F-type lectin domains also have been implicated in functions related to fertilization, protoplast regeneration, and bacterial virulence. We have recently analyzed and reported the taxonomic spread, phylogenetic distribution, architectural contexts, and sequence characteristics of prokaryotic and eukaryotic F-type lectin domains. Interestingly, while eukaryotic F-type lectin domains were frequently present as stand-alone domains, bacterial F-type lectin domains were mostly found co-occurring with enzymatic or nonenzymatic domains in diverse domain architectures, suggesting that the F-type lectin domain might be involved in targeting enzyme activities or directing other biological functions to distinct glycosylated niches in bacteria. We and others have probed the fine oligosaccharide-binding specificity of several F-type lectin domains. The currently available wealth of sequence, structural, and biochemical information about F-type lectin domains provides opportunities for the generation of designer lectins with improved binding strength and altered binding specificities. We discuss the prevalence, provenance, properties, peculiarities, and potential of F-type lectin domains for future applications in this review.

Do reef corals age?

Hydra is emerging as a model organism for studies of ageing in early metazoan animals, but reef corals offer an equally ancient evolutionary perspective as well as several advantages, not least being the hard exoskeleton which provides a rich fossil record as well as a record of growth and means of ageing of individual coral polyps. Reef corals are also widely regarded as potentially immortal at the level of the asexual lineage and are assumed not to undergo an intrinsic ageing process. However, putative molecular indicators of ageing have recently been detected in reef corals. While many of the large massive coral species attain considerable ages (>600years) there are other much shorter-lived species where older members of some populations show catastrophic mortality, compared to juveniles, under environmental stress. Other studies suggestive of ageing include those demonstrating decreased reproduction, increased susceptibility to oxidative stress and disease, reduced regeneration potential and declining growth rate in mature colonies. This review aims to promote interest and research in reef coral ageing, both as a useful model for the early evolution of ageing and as a factor in studies of ecological impacts on reef systems in light of the enhanced effects of environmental stress on ageing in other organisms.

Vertical gradients in species richness and community composition across the twilight zone in the North Pacific Subtropical Gyre

Although metazoan animals in the mesopelagic zone play critical roles in deep pelagic food webs and in the attenuation of carbon in midwaters, the diversity of these assemblages is not fully known. A metabarcoding survey of mesozooplankton diversity across the epipelagic, mesopelagic and upper bathypelagic zones (0-1500m) in the North Pacific Subtropical Gyre revealed far higher estimates of species richness than expected given prior morphology-based studies in the region (4,024 OTUs, 10-fold increase), despite conservative bioinformatic processing. Operational taxonomic unit (OTU) richness of the full assemblage peaked at lower epipelagic-upper mesopelagic depths (100-300m), with slight shoaling of maximal richness at night due to diel vertical migration, in contrast to expectations of a deep mesopelagic diversity maximum as reported for several plankton groups in early systematic and zoogeographic studies. Four distinct depth-stratified species assemblages were identified, with faunal transitions occurring at 100m, 300m and 500m. Highest diversity occurred in the smallest zooplankton size fractions (0.2-0.5mm), which had significantly lower % OTUs classified due to poor representation in reference databases, suggesting a deep reservoir of poorly understood diversity in the smallest metazoan animals. A diverse meroplankton assemblage also was detected (350 OTUs), including larvae of both shallow and deep living benthic species. Our results provide some of the first insights into the hidden diversity present in zooplankton assemblages in midwaters, and a molecular reappraisal of vertical gradients in species richness, depth distributions and community composition for the full zooplankton assemblage across the epipelagic, mesopelagic and upper bathypelagic zones.

Arthropods in the subsoil: Abundance and vertical distribution as related to soil organic matter, microbial biomass and plant roots

Large pools of organic carbon are stored in deep soil horizons (subsoil). Decomposition of soil organic matter (SOM) is driven by microorganisms that are in turn grazed by metazoan animals. Microbial populations and animal food webs in the soil are both at least partly dependent on labile organic carbon provided by plant roots. In this study, we described the vertical distribution of total Corg, microbial biomass, root biomass and the density of soil arthropods in deep layers (down to 110–210 cm depth) of three soils formed under the south taiga, broadleaved forest and forested steppe vegetation. By modeling the vertical distribution of animal population we estimated the soil depths above which 90% of the animals live (SD90 values). These values were the highest for Collembola, Protura and Symphyla (43–116, 69–144 and 54–95 cm, respectively, across the study locations), but relatively low for Acari (32–55 cm). In the forested steppe, less than 50% of all microarthropods and less than 10% of all insects inhabited litter and the uppermost 10 cm of mineral soil. Using generalized linear mixed-effect models we showed that the distribution of Collembola in the subsoil (below 30 cm) depended on root biomass and total Corg content, while the distribution of mites was affected by total Corg content and microbial biomass. The density of collembolans correlated significantly with root biomass both in the upper and lower parts of the soil profile. This suggests that soil fauna are involved in deep soil C cycling largely via grazing on root-associated microorganisms.

Specificity in diversity: single origin of a widespread ciliate-bacteria symbiosis.

Symbioses between eukaryotes and sulfur-oxidizing (thiotrophic) bacteria have convergently evolved multiple times. Although well described in at least eight classes of metazoan animals, almost nothing is known about the evolution of thiotrophic symbioses in microbial eukaryotes (protists). In this study, we characterized the symbioses between mouthless marine ciliates of the genus Kentrophoros, and their thiotrophic bacteria, using comparative sequence analysis and fluorescence in situ hybridization. Ciliate small-subunit rRNA sequences were obtained from 17 morphospecies collected in the Mediterranean and Caribbean, and symbiont sequences from 13 of these morphospecies. We discovered a new Kentrophoros morphotype where the symbiont-bearing surface is folded into pouch-like compartments, illustrating the variability of the basic body plan. Phylogenetic analyses revealed that all investigated Kentrophoros belonged to a single clade, despite the remarkable morphological diversity of these hosts. The symbionts were also monophyletic and belonged to a new clade within the Gammaproteobacteria, with no known cultured representatives. Each host morphospecies had a distinct symbiont phylotype, and statistical analyses revealed significant support for host–symbiont codiversification. Given that these symbioses were collected from two widely separated oceans, our results indicate that symbiotic associations in unicellular hosts can be highly specific and stable over long periods of evolutionary time.