Anatomy and lifestyles of Early Cambrian priapulid worms exemplified by Corynetis and Anningvermis from the Maotianshan Shale (SW China)

Accurate information on the anatomy and ecology of worms from the Cambrian Lagerstätten of SW China is sparse. The present study of two priapulid worms Anningvermis n. gen. and Corynetis Luo & Hu, 1999 from the Lower Cambrian Maotianshan Shale biota brings new information concerning the anatomical complexity, functional morphology and lifestyles of the Early Cambrian priapulids. Comparisons are made with Recent priapulids from Sweden (live observations, SEM). The cuspidate pharyngeal teeth of Anningvermis (circumoral pentagons) and the most peculiar radiating oral crown of Corynetis added to the very elongate pharynx of these two forms are interpreted as two different types of grasping apparatus possibly involved in the capture of small prey. Corynetis and Anningvermis are two representative examples of the Early Cambrian endobenthic communities largely dominated by priapulid worms (more than ten species in the Maotianshan Shale biota) and to a much lesser extent by brachiopods. Corynetis and Anningvermis were probably active mud-burrowers and predators of small meiobenthic animals. Likewise predator priapulid worms exploited the interface layer between the seawater and bottom sediment, where meiobenthic organisms were abundant and functioned as prey. This implies that complex prey-predator relationship between communities already existed in the Early Cambrian. This study also shows that the circumoral pentagonal teeth and caudal appendage were present in the early stages of the evolutionary history of the group and were important features of the priapulid body plan already in the Early Cambrian. Two new families, one new genus and new species are introduced and described in the appendix.     

The macro‐ and microfossil record of the Cambrian priapulid Ottoia

The stem‐group priapulid Ottoia Walcott, 1911, is the most abundant worm in the mid‐Cambrian Burgess Shale, but has not been unambiguously demonstrated elsewhere. High‐resolution electron and optical microscopy of macroscopic Burgess Shale specimens reveals the detailed anatomy of its robust hooks, spines and pharyngeal teeth, establishing the presence of two species: Ottoia prolifica Walcott, 1911, and Ottoia tricuspida sp. nov. Direct comparison of these sclerotized elements with a suite of shale‐hosted mid‐to‐late Cambrian microfossils extends the range of ottoiid priapulids throughout the middle to upper Cambrian strata of the Western Canada Sedimentary Basin. Ottoiid priapulids represented an important component of Cambrian ecosystems: they occur in a range of lithologies and thrived in shallow water as well as in the deep‐water setting of the Burgess Shale. A wider survey of Burgess Shale macrofossils reveals specific characters that diagnose priapulid sclerites more generally, establishing the affinity of a wide range of Small Carbonaceous Fossils and demonstrating the prominent role of priapulids in Cambrian seas.     

Early embryonic development of the priapulid worm Priapulus caudatus

SUMMARY The early cleavage up to gastrulation is described here for the priapulid worm Priapulus caudatus , contradicting and clarifying earlier partial reports on this topic. The cleavage pattern up to gastrulation is highly symmetrical, total, subequal, radial, and stereotypical. Gastrulation is intermediate between epiboly and invagination, and the mesendoderm may be derived from both cells of the first cleavage, thus differing significantly in its origin from that of many other protostomes. Priapulids occupy an increasingly important position in studies of animal evolution as they appear to be relatively basal within the new clade Ecdysozoa (panarthropods plus cycloneuralians); and have been described as both morphological and genetic living fossils. The insights derived from priapulids combined with new data published recently on kinorhynchs and tardigrades imply a substantial developmental diversity among basal ecdysozoans, and weakens the hypothesis that irregular cleavage is plesiomorphic to the entire clade. Further study is required to reconstruct basal cleavage patterns in both this clade, and indeed, the Bilateria as a whole.     

The complete mitochondrial genome of the onychophoran Epiperipatus biolleyi reveals a unique transfer RNA set and provides further support for the ecdysozoa hypothesis

Onychophora (velvet worms) play a crucial role in current discussions on position of arthropods. The ongoing Articulata/Ecdysozoa debate is in need of additional ground pattern characters for Panarthropoda (Arthropoda, Tardigrada, and Onychophora). Hence, Onychophora is an important outgroup taxon in resolving the relationships among arthropods, irrespective of whether morphological or molecular data are used. To date, there has been a noticeable lack of mitochondrial genome data from onychophorans. Here, we present the first complete mitochondrial genome sequence of an onychophoran, Epiperipatus biolleyi (Peripatidae), which shows several characteristic features. Specifically, the gene order is considerably different from that in other arthropods and other bilaterians. In addition, there is a lack of 9 tRNA genes usually present in bilaterian mitochondrial genomes. All these missing tRNAs have anticodon sequences corresponding to 4-fold degenerate codons, whereas the persisting 13 tRNAs all have anticodons pairing with 2-fold degenerate codons. Sequence-based phylogenetic analysis of the mitochondrial protein-coding genes provides a robust support for a clade consisting of Onychophora, Priapulida, and Arthropoda, which confirms the Ecdysozoa hypothesis. However, resolution of the internal ecdysozoan relationships suffers from a cluster of long-branching taxa (including Nematoda and Platyhelminthes) and a lack of data from Tardigrada and further nemathelminth taxa in addition to nematodes and priapulids.     

The Mitochondrial Genome of Soybean Reveals Complex Genome Structures and Gene Evolution at Intercellular and Phylogenetic Levels

Determining mitochondrial genomes is important for elucidating vital activities of seed plants. Mitochondrial genomes are specific to each plant species because of their variable size, complex structures and patterns of gene losses and gains during evolution. This complexity has made research on the soybean mitochondrial genome difficult compared with its nuclear and chloroplast genomes. The present study helps to solve a 30-year mystery regarding the most complex mitochondrial genome structure, showing that pairwise rearrangements among the many large repeats may produce an enriched molecular pool of 760 circles in seed plants. The soybean mitochondrial genome harbors 58 genes of known function in addition to 52 predicted open reading frames of unknown function. The genome contains sequences of multiple identifiable origins, including 6.8 kb and 7.1 kb DNA fragments that have been transferred from the nuclear and chloroplast genomes, respectively, and some horizontal DNA transfers. The soybean mitochondrial genome has lost 16 genes, including nine protein-coding genes and seven tRNA genes; however, it has acquired five chloroplast-derived genes during evolution. Four tRNA genes, common among the three genomes, are derived from the chloroplast. Sizeable DNA transfers to the nucleus, with pericentromeric regions as hotspots, are observed, including DNA transfers of 125.0 kb and 151.6 kb identified unambiguously from the soybean mitochondrial and chloroplast genomes, respectively. The soybean nuclear genome has acquired five genes from its mitochondrial genome. These results provide biological insights into the mitochondrial genome of seed plants, and are especially helpful for deciphering vital activities in soybean.     

A cryptic record of Burgess Shale‐type diversity from the early Cambrian of Baltica

Exceptionally preserved ‘Burgess Shale‐type’ fossil assemblages from the Cambrian of Laurentia, South China and Australia record a diverse array of non‐biomineralizing organisms. During this time, the palaeocontinent Baltica was geographically isolated from these regions, and is conspicuously lacking in terms of comparable accessible early Cambrian Lagerstätten. Here we report a diverse assemblage of small carbonaceous fossils (SCFs) from the early Cambrian (Stage 4) File Haidar Formation of southeast Sweden and surrounding areas of the Baltoscandian Basin, including exceptionally preserved remains of Burgess Shale‐type metazoans and other organisms. Recovered SCFs include taxonomically resolvable ecdysozoan elements (priapulid and palaeoscolecid worms), lophotrochozoan elements (annelid chaetae and wiwaxiid sclerites), as well as ‘protoconodonts’, denticulate feeding structures, and a background of filamentous and spheroidal microbes. The annelids, wiwaxiids and priapulids are the first recorded from the Cambrian of Baltica. The File Haidar SCF assemblage is broadly comparable to those recovered from Cambrian basins in Laurentia and South China, though differences at lower taxonomic levels point to possible environmental or palaeogeographical controls on taxon ranges. These data reveal a fundamentally expanded picture of early Cambrian diversity on Baltica, and provide key insights into high‐latitude Cambrian faunas and patterns of SCF preservation. We establish three new taxa based on large populations of distinctive SCFs: Baltiscalida njorda gen. et sp. nov. (a priapulid), Baltichaeta jormunganda gen. et sp. nov. (an annelid) and Baltinema rana gen. et sp. nov. (a filamentous problematicum).     

Predation by early Cambrian trilobites on infaunal worms - evidence from the Swedish Mickwitzia Sandstone

Evidence of early Cambrian predation is found in trace fossils from the Mickwitzia Sandstone of VastergÖtland, Sweden. The arthropod burrow Rusophycw dispar was dug down to spreite burrows in such a manner that mere coincidence of place is unlikely. The predator is identified as an olenellacean trilobite, mainly through the presence of a cephalic impression. The prey, a worm that may have been a priapulid, was localized visually or chemically at the spreite-burrows apertures. The predator lacked legs specialized for seizing prey, as indicated by the parallel, but laterally displaced position of the Rusophycus above the spreite burrow. In this stance prey could be gripped by flexing the supposedly spinose legs of one side around it. When a spreite burrow of limited horizontal extension was encountered, parallel orientation was obtained prior to digging, probably through chemical sensing, whereas parallel orientation to an extended burrow required a number of diggings. These traces are important evidence of early Cambrian predation and of the predatorial capability of trilobites. □ Lower Cambrian, Sweden predation, trilobites, priapulids , Rusophycus.     

Community palaeoecology of the early Cambrian Maotianshan Shale biota: Ecological dominance of priapulid worms

The early Cambrian soft-bodied Maotianshan Shale (Chengjiang) biota of Yunnan Province, China provides a critical glimpse of animal life during the heart of the Cambrian radiation. The Shankou biota is the focus of this current work, and 9963 specimens from it have been examined and tallied. This collection of fossils represents a time-averaged assemblage of unknown duration from a 10-meter thick sequence. The predominantly benthic community recovered from this section is presumably autochthonous. This community was buried through several hundred millimeter to centimeter thick burial events. Only specimens interpreted as buried alive, based on either soft-part preservation or fully articulated skeletons, were counted. Algae were too fragmented to be counted. To avoid including synonymous species, diversity was evaluated at the genus level. A total of 57 genera from 9 phyla, encompassing 14 ecological groups, were found in this assemblage. The results reveal that the three most abundant genera comprise 43.2% of all specimens: the tubiform priapulid worm Paraselkirkia (16.0%), the diminutive priapulid worm Sicyophorus (14.3%), and the brachiopod Heliomedusa (12.9%). No other genera total more than 9% of specimens. At the phylum level, there is an interesting dichotomy between taxonomic diversity and ecological dominance. The arthropods are the most diverse phylum (37% of genera) and rank second in relative abundance of specimens (26.3%). The priapulids, however, with only 17.5% of genera is the most abundant group in the assemblage (43.2%). All other phyla, excluding brachiopods (19.6%), represent only 10.9% of the assemblage. Because of their sheer numerical abundance, this study indicates that priapulid worms may have exerted more influence on energy flow and community structure than other phyla in this particular trophic web. This result contrasts strongly with both traditional views of Maotianshan Shale biota palaeoecology, which often claimed arthropod dominance based solely on taxonomic diversity, and the palaeoecology of modern priapulids, which are relegated to marginal marine settings. This result also demonstrates the importance of collecting quantitative relative abundance data when performing palaeoecological investigations.     

Rapid structural evolution of Dendrobium mitogenomes and mito-nuclear phylogeny discordances in Dendrobium (Orchidaceae)

Reconstructing mitochondrial genomes of angiosperms is extremely intricate due to frequent recombinations which give rise to varied sized in Dendrobium mitogenomes and their structural variations, even in most orchid species. In this study, we first sequenced two complete and five draft mitochondrial genomes of Dendrobium using next-generation and third-generation sequencing technologies. The mitochondrial genomes were 420 538–689 048 bp long, showing multipartite (multichromosomal) structures that consisted of variably sized circular or linear-mapping isoforms (chromosomes). The comparison of mitochondrial genomes showed frequent gene losses in Dendrobium species. To explore structure variations of mitochondrial genomes in vivo, we quantified copy numbers of five mitochondrial genes and DNA contents per mitochondrion. The gene copy numbers and the DNA contents showed extreme differences during Dendrobium development, suggesting dynamic structures of mitochondrial genomes. Furthermore, phylogenetic relationships of 97 accessions from 39 Dendrobium species were constructed based on 12 nuclear single-copy genes and 15 mitochondrial genes. We discovered obvious discordance between the nuclear and mitochondrial trees. Reticulate evolution was inferred from the species network analysis in Dendrobium. Our findings revealed the rapid structural evolution of Dendrobium mitochondrial genomes and the existence of hybridization events in Dendrobium species, which provided new insights into in vivo structural variations of plant mitochondrial genomes and the strong potential of mitochondrial genes in deciphering plant evolution history.     

Recent Priapulidae and their Early Cambrian ancestors: comparisons and evolutionary significance

Although priapulid worms form a relatively small phylum in present-day marine environments, they were important animals in Cambrian endobenthic communities. Two Early Cambrian priapulids, namely Xiaoheiqingella peculiaris and Yunnanpriapulus halteroformis nov. gen., nov. sp. from the Maotianshan Shale Lagerstätte of SW China are revised and described. Several key-features of the body plan of Recent Priapulidae are recognized in these two forms: 1) the four-fold body division (introvert, neck, trunk, and caudal appendage); 2) the well-developed introvert armed with ca. 25 longitudinal rows of scalids; 3) the caudal appendage; 4) the pharyngeal teeth arranged in a pentagonal disposition (Xiaoheiqingella); 5) the ventral nerve cord present in Yunnanpriapulus. This morphology indicates close evolutionary relationships with modern priapulids. Xiaoheiqingella and Yunnanpriapulus nov. gen. are tentatively placed within the recent family Priapulidae. The Priapulidae lineage may therefore have a remote origin (Early Cambrian) much older than was previously assumed (Priapulites; Late Carboniferous). The functional morphology of Xiaoheiqingella and Yunnanpriapulus nov. gen. suggests that these two worms were chiefly carnivorous with possible occasional mud-eating habits.     

Dynamic evolution of eukaryotic mitochondrial and nuclear genomes: a case study in the gourmet pine mushroom Tricholoma matsutake

Fungi, as eukaryotic organisms, contain two genomes, the mitochondrial genome and the nuclear genome, in their cells. How the two genomes evolve and correlate to each other is debated. Herein, taking the gourmet pine mushroom Tricholoma matsutake as an example, we performed comparative mitogenomic analysis using samples collected from diverse locations and compared the evolution of the two genomes. The T. matsutake mitogenome encodes 49 genes and is rich of repetitive and non-coding DNAs. Six genes were invaded by up to 11 group I introns, with one cox1 intron cox1P372 showing presence/absence dynamics among different samples. Bioinformatic analyses suggested limited or no evidence of mitochondrial heteroplasmy. Interestingly, hundreds of mitochondrial DNA fragments were found in the nuclear genome, with several larger than 500 nt confirmed by PCR assays and read count comparisons, indicating clear evidence of transfer of mitochondrial DNA into the nuclear genome. Nuclear DNA of T. matsutake showed a higher mutation rate than mitochondrial DNA. Furthermore, we found evidence of incongruence between phylogenetic trees derived from mitogenome and nuclear DNA sequences. Together, our results reveal the dynamic genome evolution of the gourmet pine mushroom.     

The evolution of the Ecdysozoa

Ecdysozoa is a clade composed of eight phyla: the arthropods, tardigrades and onychophorans that share segmentation and appendages and the nematodes, nematomorphs, priapulids, kinorhynchs and loriciferans, which are worms with an anterior proboscis or introvert. Ecdysozoa contains the vast majority of animal species and there is a great diversity of body plans among both living and fossil members. The monophyly of the clade has been called into question by some workers based on analyses of whole genome datasets. We review the evidence that now conclusively supports the unique origin of these phyla. Relationships within Ecdysozoa are also controversial and we discuss the molecular and morphological evidence for a number of monophyletic groups within this superphylum.     

The larval nervous system of the penis worm Priapulus caudatus (Ecdysozoa)

The origin and extreme diversification of the animal nervous system is a central question in biology. While most of the attention has traditionally been paid to those lineages with highly elaborated nervous systems (e.g. arthropods, vertebrates, annelids), only the study of the vast animal diversity can deliver a comprehensive view of the evolutionary history of this organ system. In this regard, the phylogenetic position and apparently conservative molecular, morphological and embryological features of priapulid worms (Priapulida) place this animal lineage as a key to understanding the evolution of the Ecdysozoa (i.e. arthropods and nematodes). In this study, we characterize the nervous system of the hatching larva and first lorica larva of the priapulid worm Priapulus caudatus by immunolabelling against acetylated and tyrosinated tubulin, pCaMKII, serotonin and FMRFamide. Our results show that a circumoral brain and an unpaired ventral nerve with a caudal ganglion characterize the central nervous system of hatching embryos. After the first moult, the larva attains some adult features: a neck ganglion, an introvert plexus, and conspicuous secondary longitudinal neurites. Our study delivers a neuroanatomical framework for future embryological studies in priapulid worms, and helps illuminate the course of nervous system evolution in the Ecdysozoa.     

Evolution of mitochondrial genomes and the genetic code.

Mitochondrial genomes are clearly marked by a strong tendency towards reductive evolution. This tendency has been facilitated by the transfer of most of the essential genes for mitochondrial propogation and function to the nuclear genome. The most extreme examples of genomic simplification are seen in animal mitochondria, where there also are the greatest tendencies to codon reassignment. The reassignment of codons to amino acids different from those designated in the so called universal code is seen in part as an expression of the reduction of the number of genes used by these genomes to code for tRNA species. The driving force for the reductive evolution of mitochondrial genomes is identified with two population genetic effects which may also be operating on populations of parasites.     

Mitochondrial genome sequence evolution in Chlamydomonas

The mitochondrial genomes of the Chlorophyta exhibit significant diversity with respect to gene content and genome compactness; however, quantitative data on the rates of nucleotide substitution in mitochondrial DNA, which might help explain the origin of this diversity, are lacking. To gain insight into the evolutionary forces responsible for mitochondrial genome diversification, we sequenced to near completion the mitochondrial genome of the chlorophyte Chlamydomonas incerta, estimated the evolutionary divergence between Chlamydomonas reinhardtii and C. incerta mitochondrial protein-coding genes and rRNA-coding regions, and compared the relative evolutionary rates in mitochondrial and nuclear genes. Synonymous and nonsynonymous substitution rates do not differ significantly between the mitochondrial and nuclear protein-coding genes. The mitochondrial rRNA-coding regions, however, are evolving much faster than their nuclear counterparts, and this difference might be explained by relaxed functional constraints on the mitochondrial translational apparatus due to the small number of proteins synthesized in Chlamydomonas mitochondria. Substitution rates at synonymous sites in a nonstandard mitochondrial gene (rtl) and at intronic and synonymous sites in nuclear genes expressed at low levels suggest that the mutation rate is similar in these two genetic compartments. Potential evolutionary forces shaping mitochondrial genome evolution in Chlamydomonas are discussed.     

Horizontal gene transfer in plants

Horizontal gene transfer (HGT) has played a major role in bacterial evolution and is fairly common in certain unicellular eukaryotes. However, the prevalence and importance of HGT in the evolution of multicellular eukaryotes remain unclear. Recent studies indicate that plant mitochondrial genomes are unusually active in HGT relative to all other organellar and nuclear genomes of multicellular eukaryotes. Although little about the mechanisms of plant HGT is known, several studies have implicated parasitic plants as both donors and recipients of mitochondrial genes. Most cases uncovered thus far have involved a single transferred gene per species; however, recent work has uncovered a case of massive HGT in Amborella trichopoda involving acquisition of at least a few dozen and probably hundreds of foreign mitochondrial genes. These foreign genes came from multiple donors, primarily eudicots and mosses. This review will examine the implications of such massive transfer, the potential mechanisms and consequences of plant-to-plant mitochondrial HGT in general, as well as the limited evidence for HGT in plant chloroplast and nuclear genomes.     

Genome compaction and stability in microsporidian intracellular parasites

Microsporidian genomes are extraordinary among eukaryotes for their extreme reduction: although they are similar in form to other eukaryotic genomes, they are typically smaller than many prokaryotic genomes. At the same time, their rates of sequence evolution are among the highest for eukaryotic organisms. To explore the effects of compaction on nuclear genome evolution, we sequenced 685,000 bp of the Antonospora locustae genome (formerly Nosema locustae) and compared its organization with the recently completed genome of the human parasite Encephalitozoon cuniculi. Despite being very distantly related, the genomes of these two microsporidian species have retained an unexpected degree of synteny: 13% of genes are in the same context, and 30% of the genes were separated by a small number of short rearrangements. Microsporidian genomes are, therefore, paradoxically composed of rapidly evolving sequences harbored within a slowly evolving genome, although these two processes are sometimes considered to be coupled. Microsporidian genomes show that eukaryotic genomes (like genes) do not evolve in a clock-like fashion, and genome stability may result from compaction in addition to a lack of recombination, as has been traditionally thought to occur in bacterial and organelle genomes.     

Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates

Genome size and complexity vary tremendously among eukaryotic species and their organelles. Comparisons across deeply divergent eukaryotic lineages have suggested that variation in mutation rates may explain this diversity, with increased mutational burdens favoring reduced genome size and complexity. The discovery that mitochondrial mutation rates can differ by orders of magnitude among closely related angiosperm species presents a unique opportunity to test this hypothesis. We sequenced the mitochondrial genomes from two species in the angiosperm genus Silene with recent and dramatic accelerations in their mitochondrial mutation rates. Contrary to theoretical predictions, these genomes have experienced a massive proliferation of noncoding content. At 6.7 and 11.3 Mb, they are by far the largest known mitochondrial genomes, larger than most bacterial genomes and even some nuclear genomes. In contrast, two slowly evolving Silene mitochondrial genomes are smaller than average for angiosperms. Consequently, this genus captures approximately 98% of known variation in organelle genome size. The expanded genomes reveal several architectural changes, including the evolution of complex multichromosomal structures (with 59 and 128 circular-mapping chromosomes, ranging in size from 44 to 192 kb). They also exhibit a substantial reduction in recombination and gene conversion activity as measured by the relative frequency of alternative genome conformations and the level of sequence divergence between repeat copies. The evolution of mutation rate, genome size, and chromosome structure can therefore be extremely rapid and interrelated in ways not predicted by current evolutionary theories. Our results raise the hypothesis that changes in recombinational processes, including gene conversion, may be a central force driving the evolution of both mutation rate and genome structure.     

The Mitochondrial Genome of Raphanus sativus and Gene Evolution of Cruciferous Mitochondrial Types

To explore the mitochondrial genes of the Cruciferae family, the mitochondrial genome of Raphanus sativus (sat) was sequenced and annotated. The circular mitochondrial genome of sat is 239,723 bp and includes 33 protein-coding genes, three rRNA genes and 17 tRNA genes. The mitochondrial genome also contains a pair of large repeat sequences 5.9 kb in length, which may mediate genome reorga-nization into two sub-genomic circles, with predicted sizes of 124.8 kb and 115.0 kb, respectively. Furthermore, gene evolution of mitochondrial genomes within the Cruciferae family was analyzed using sat mitochondrial type (mitotype), together with six other re-ported mitotypes. The cruciferous mitochondrial genomes have maintained almost the same set of functional genes. Compared with Cycas taitungensis (a representative gymnosperm), the mitochondrial genomes of the Cruciferae have lost nine protein-coding genes and seven mitochondrial-like tRNA genes, but acquired six chloroplast-like tRNAs. Among the Cruciferae, to maintain the same set of genes that are necessary for mitochondrial function, the exons of the genes have changed at the lowest rates, as indicated by the numbers of single nucleotide polymorphisms. The open reading frames (ORFs) of unknown function in the cruciferous genomes are not conserved. Evolutionary events, such as mutations, genome reorganizations and sequence insertions or deletions (indels), have resulted in the non- conserved ORFs in the cruciferous mitochondrial genomes, which is becoming significantly different among mitotypes. This work represents the first phylogenic explanation of the evolution of genes of known function in the Cruciferae family. It revealed significant variation in ORFs and the causes of such variation.