Biogeochemical and microbial variation across 5500 km of Antarctic surface sediment implicates organic matter as a driver of Benthic Community Structure.

This is the final version of the article. Available from Frontiers Media via the DOI in this record.Western Antarctica, one of the fastest warming locations on Earth, is a unique environment that is underexplored with regards to biodiversity. Although pelagic microbial communities in the Southern Ocean and coastal Antarctic waters have been well-studied, there are fewer investigations of benthic communities and most have a focused geographic range. We sampled surface sediment from 24 sites across a 5500 km region of Western Antarctica (covering the Ross Sea to the Weddell Sea) to examine relationships between microbial communities and sediment geochemistry. Sequencing of the 16S and 18S rRNA genes showed microbial communities in sediments from the Antarctic Peninsula (AP) and Western Antarctica (WA), including the Ross, Amundsen, and Bellingshausen Seas, could be distinguished by correlations with organic matter concentrations and stable isotope fractionation (total organic carbon; TOC, total nitrogen; TN, and δ(13)C). Overall, samples from the AP were higher in nutrient content (TOC, TN, and NH4 (+)) and communities in these samples had higher relative abundances of operational taxonomic units (OTUs) classified as the diatom, Chaetoceros, a marine cercozoan, and four OTUs classified as Flammeovirgaceae or Flavobacteria. As these OTUs were strongly correlated with TOC, the data suggests the diatoms could be a source of organic matter and the Bacteroidetes and cercozoan are grazers that consume the organic matter. Additionally, samples from WA have lower nutrients and were dominated by Thaumarchaeota, which could be related to their known ability to thrive as lithotrophs. This study documents the largest analysis of benthic microbial communities to date in the Southern Ocean, representing almost half the continental shoreline of Antarctica, and documents trophic interactions and coupling of pelagic and benthic communities. Our results indicate potential modifications in carbon sequestration processes related to change in community composition, identifying a prospective mechanism that links climate change to carbon availability.Funds through NSF Antarctic Program: AM (CMU: Award Number 1043670), KH, and SS (AU Award Number: 1043745) and from Central Michigan University Faculty Research and Creative Endeavors (FRCE) Committee and College of Science and Technolog

Annelid phylogeny and the status of Sipuncula and Echiura

BACKGROUND: Annelida comprises an ancient and ecologically important animal phylum with over 16,500 described species and members are the dominant macrofauna of the deep sea. Traditionally, two major groups are distinguished: Clitellata (including earthworms, leeches) and "Polychaeta" (mostly marine worms). Recent analyses of molecular data suggest that Annelida may include other taxa once considered separate phyla (i.e., Echiura, and Sipuncula) and that Clitellata are derived annelids, thus rendering "Polychaeta" paraphyletic; however, this contradicts classification schemes of annelids developed from recent analyses of morphological characters. Given that deep-level evolutionary relationships of Annelida are poorly understood, we have analyzed comprehensive datasets based on nuclear and mitochondrial genes, and have applied rigorous testing of alternative hypotheses so that we can move towards the robust reconstruction of annelid history needed to interpret animal body plan evolution. RESULTS: Sipuncula, Echiura, Siboglinidae, and Clitellata are all nested within polychaete annelids according to phylogenetic analyses of three nuclear genes (18S rRNA, 28S rRNA, EF1α; 4552 nucleotide positions analyzed) for 81 taxa, and 11 nuclear and mitochondrial genes for 10 taxa (additional: 12S rRNA, 16S rRNA, ATP8, COX1-3, CYTB, NAD6; 11,454 nucleotide positions analyzed). For the first time, these findings are substantiated using approximately unbiased tests and non-scaled bootstrap probability tests that compare alternative hypotheses. For echiurans, the polychaete group Capitellidae is corroborated as the sister taxon; while the exact placement of Sipuncula within Annelida is still uncertain, our analyses suggest an affiliation with terebellimorphs. Siboglinids are in a clade with other sabellimorphs, and clitellates fall within a polychaete clade with aeolosomatids as their possible sister group. None of our analyses support the major polychaete clades reflected in the current classification scheme of annelids, and hypothesis testing significantly rejects monophyly of Scolecida, Palpata, Canalipalpata, and Aciculata. CONCLUSION: Using multiple genes and explicit hypothesis testing, we show that Echiura, Siboglinidae, and Clitellata are derived annelids with polychaete sister taxa, and that Sipuncula should be included within annelids. The traditional composition of Annelida greatly underestimates the morphological diversity of this group, and inclusion of Sipuncula and Echiura implies that patterns of segmentation within annelids have been evolutionarily labile. Relationships within Annelida based on our analyses of multiple genes challenge the current classification scheme, and some alternative hypotheses are provided

The Effect of a DNA Damaging Agent on Embryonic Cell Cycles of the Cnidarian Hydractinia echinata

The onset of gastrulation at the Mid-Blastula Transition can accompany profound changes in embryonic cell cycles including the introduction of gap phases and the transition from maternal to zygotic control. Studies in Xenopus and Drosophila embryos have also found that cell cycles respond to DNA damage differently before and after MBT (or its equivalent, MZT, in Drosophila). DNA checkpoints are absent in Xenopus cleavage cycles but are acquired during MBT. Drosophila cleavage nuclei enter an abortive mitosis in the presence of DNA damage whereas post-MZT cells delay the entry into mitosis. Despite attributes that render them workhorses of embryonic cell cycle studies, Xenopus and Drosophila are hardly representative of diverse animal forms that exist. To investigate developmental changes in DNA damage responses in a distant phylum, I studied the effect of an alkylating agent, Methyl Methanesulfonate (MMS), on embryos of Hydractinia echinata. Hydractinia embryos are found to differ from Xenopus embryos in the ability to respond to a DNA damaging agent in early cleavage but are similar to Xenopus and Drosophila embryos in acquiring stronger DNA damage responses and greater resistance to killing by MMS after the onset of gastrulation. This represents the first study of DNA damage responses in the phylum Cnidaria

The complete mitochondrial genome of Flustra foliacea (Ectoprocta, Cheilostomata) - compositional bias affects phylogenetic analyses of lophotrochozoan relationships

<p>Abstract</p> <p>Background</p> <p>The phylogenetic relationships of the lophophorate lineages, ectoprocts, brachiopods and phoronids, within Lophotrochozoa are still controversial. We sequenced an additional mitochondrial genome of the most species-rich lophophorate lineage, the ectoprocts. Although it is known that there are large differences in the nucleotide composition of mitochondrial sequences of different lineages as well as in the amino acid composition of the encoded proteins, this bias is often not considered in phylogenetic analyses. We applied several approaches for reducing compositional bias and saturation in the phylogenetic analyses of the mitochondrial sequences.</p> <p>Results</p> <p>The complete mitochondrial genome (16,089 bp) of <it>Flustra foliacea </it>(Ectoprocta, Gymnolaemata, Cheilostomata) was sequenced. All protein-encoding, rRNA and tRNA genes are transcribed from the same strand. <it>Flustra </it>shares long intergenic sequences with the cheilostomate ectoproct <it>Bugula</it>, which might be a synapomorphy of these taxa. Further synapomorphies might be the loss of the DHU arm of the tRNA L(UUR), the loss of the DHU arm of the tRNA S(UCN) and the unique anticodon sequence GAG of the tRNA L(CUN). The gene order of the mitochondrial genome of <it>Flustra </it>differs strongly from that of the other known ectoprocts. Phylogenetic analyses of mitochondrial nucleotide and amino acid data sets show that the lophophorate lineages are more closely related to trochozoan phyla than to deuterostomes or ecdysozoans confirming the Lophotrochozoa hypothesis. Furthermore, they support the monophyly of Cheilostomata and Ectoprocta. However, the relationships of the lophophorate lineages within Lophotrochozoa differ strongly depending on the data set and the used method. Different approaches for reducing heterogeneity in nucleotide and amino acid data sets and saturation did not result in a more robust resolution of lophotrochozoan relationships.</p> <p>Conclusion</p> <p>The contradictory and usually weakly supported phylogenetic reconstructions of the relationships among lophotrochozoan phyla based on mitochondrial sequences indicate that these alone do not contain enough information for a robust resolution of the relations of the lophotrochozoan phyla. The mitochondrial gene order is also not useful for inferring their phylogenetic relationships, because it is highly variable in ectoprocts, brachiopods and some other lophotrochozoan phyla. However, our study revealed several rare genomic changes like the evolution of long intergenic sequences and changes in the structure of tRNAs, which may be helpful for reconstructing ectoproct phylogeny.</p

Acoel Flatworms Are Not Platyhelminthes: Evidence from Phylogenomics

Acoel flatworms are small marine worms traditionally considered to belong to the phylum Platyhelminthes. However, molecular phylogenetic analyses suggest that acoels are not members of Platyhelminthes, but are rather extant members of the earliest diverging Bilateria. This result has been called into question, under suspicions of a long branch attraction (LBA) artefact. Here we re-examine this problem through a phylogenomic approach using 68 different protein-coding genes from the acoel Convoluta pulchra and 51 metazoan species belonging to 15 different phyla. We employ a mixture model, named CAT, previously found to overcome LBA artefacts where classical models fail. Our results unequivocally show that acoels are not part of the classically defined Platyhelminthes, making the latter polyphyletic. Moreover, they indicate a deuterostome affinity for acoels, potentially as a sister group to all deuterostomes, to Xenoturbellida, to Ambulacraria, or even to chordates. However, the weak support found for most deuterostome nodes, together with the very fast evolutionary rate of the acoel Convoluta pulchra, call for more data from slowly evolving acoels (or from its sister-group, the Nemertodermatida) to solve this challenging phylogenetic problem

Barcoding of Arrow Worms (Phylum Chaetognatha) from Three Oceans: Genetic Diversity and Evolution within an Enigmatic Phylum

Arrow worms (Phylum Chaetognatha) are abundant planktonic organisms and important predators in many food webs; yet, the classification and evolutionary relationships among chaetognath species remain poorly understood. A seemingly simple body plan is underlain by subtle variation in morphological details, obscuring the affinities of species within the phylum. Many species achieve near global distributions, spanning the same latitudinal bands in all ocean basins, while others present disjunct ranges, in some cases with the same species apparently found at both poles. To better understand how these complex evolutionary and geographic variables are reflected in the species makeup of chaetognaths, we analyze DNA barcodes of the mitochondrial cytochrome oxidase c subunit I (COI) gene, from 52 specimens of 14 species of chaetognaths collected mainly from the Atlantic Ocean. Barcoding analysis was highly successful at discriminating described species of chaetognaths across the phylum, and revealed little geographical structure. This barcode analysis reveals hitherto unseen genetic variation among species of arrow worms, and provides insight into some species relationships of this enigmatic group

Reticulate evolution: frequent introgressive hybridization among chinese hares (genus lepus) revealed by analyses of multiple mitochondrial and nuclear DNA loci

<p>Abstract</p> <p>Background</p> <p>Interspecific hybridization may lead to the introgression of genes and genomes across species barriers and contribute to a reticulate evolutionary pattern and thus taxonomic uncertainties. Since several previous studies have demonstrated that introgressive hybridization has occurred among some species within <it>Lepus</it>, therefore it is possible that introgressive hybridization events also occur among Chinese <it>Lepus </it>species and contribute to the current taxonomic confusion.</p> <p>Results</p> <p>Data from four mtDNA genes, from 116 individuals, and one nuclear gene, from 119 individuals, provides the first evidence of frequent introgression events via historical and recent interspecific hybridizations among six Chinese <it>Lepus </it>species. Remarkably, the mtDNA of <it>L. mandshuricus </it>was completely replaced by mtDNA from <it>L. timidus </it>and <it>L. sinensis</it>. Analysis of the nuclear DNA sequence revealed a high proportion of heterozygous genotypes containing alleles from two divergent clades and that several haplotypes were shared among species, suggesting repeated and recent introgression. Furthermore, results from the present analyses suggest that Chinese hares belong to eight species.</p> <p>Conclusion</p> <p>This study provides a framework for understanding the patterns of speciation and the taxonomy of this clade. The existence of morphological intermediates and atypical mitochondrial gene genealogies resulting from frequent hybridization events likely contribute to the current taxonomic confusion of Chinese hares. The present study also demonstrated that nuclear gene sequence could offer a powerful complementary data set with mtDNA in tracing a complete evolutionary history of recently diverged species.</p

Dancing for Food in the Deep Sea: Bacterial Farming by a New Species of Yeti Crab

Vent and seep animals harness chemosynthetic energy to thrive far from the sun's energy. While symbiont-derived energy fuels many taxa, vent crustaceans have remained an enigma; these shrimps, crabs, and barnacles possess a phylogenetically distinct group of chemosynthetic bacterial epibionts, yet the role of these bacteria has remained unclear. We test whether a new species of Yeti crab, which we describe as Kiwa puravida n. sp, farms the epibiotic bacteria that it grows on its chelipeds (claws), chelipeds that the crab waves in fluid escaping from a deep-sea methane seep. Lipid and isotope analyses provide evidence that epibiotic bacteria are the crab's main food source and K. puravida n. sp. has highly-modified setae (hairs) on its 3rd maxilliped (a mouth appendage) which it uses to harvest these bacteria. The ε- and γ- proteobacteria that this methane-seep species farms are closely related to hydrothermal-vent decapod epibionts. We hypothesize that this species waves its arm in reducing fluid to increase the productivity of its epibionts by removing boundary layers which may otherwise limit carbon fixation. The discovery of this new species, only the second within a family described in 2005, stresses how much remains undiscovered on our continental margins

Acoelomorpha: earliest branching bilaterians or deuterostomes?

The Acoelomorpha is an animal group comprised by nearly 400 species of misleadingly inconspicuous flatworms. Despite this, acoelomorphs have been at the centre of a heated debate about the origin of bilaterian animals for 150 years. The animal tree of life has undergone major changes during the last decades, thanks largely to the advent of molecular data together with the development of more rigorous phylogenetic methods. There is now a relatively robust backbone of the animal tree of life. However, some crucial nodes remain contentious, especially the node defining the root of Bilateria. Some studies situate Acoelomorpha (and Xenoturbellida) as the sister group of all other bilaterians, while other analyses group them within the deuterostomes which instead suggests that the last common bilaterian ancestor directly gave rise to deuterostomes and protostomes. The resolution of this node will have a profound impact on our understanding of animal/bilaterian evolution. In particular, if acoelomorphs are the sister group to Bilateria, it will point to a simple nature for the first bilaterian. Alternatively, if acoelomorphs are deuterostomes, this will imply that they are the result of secondary simplification. Here, we review the state of this question and provide potential ways to solve this long-standing issue. Specifically, we argue for the benefits of (1) obtaining additional genomic data from acoelomorphs, in particular from taxa with slower evolutionary rates; (2) the development of new tools to analyse the data; and (3) the use of metagenomics or metatranscriptomics data. We believe the combination of these three approaches will provide a definitive answer as to the position of the acoelomorphs in the animal tree of life

The enigmatic mitochondrial genome of Rhabdopleura compacta (Pterobranchia) reveals insights into selection of an efficient tRNA system and supports monophyly of Ambulacraria

<p>Abstract</p> <p>Background</p> <p>The Hemichordata comprises solitary-living Enteropneusta and colonial-living Pterobranchia, sharing morphological features with both Chordata and Echinodermata. Despite their key role for understanding deuterostome evolution, hemichordate phylogeny is controversial and only few molecular data are available for phylogenetic analysis. Furthermore, mitochondrial sequences are completely lacking for pterobranchs. Therefore, we determined and analyzed the complete mitochondrial genome of the pterobranch <it>Rhabdopleura compacta </it>to elucidate deuterostome evolution. Thereby, we also gained important insights in mitochondrial tRNA evolution.</p> <p>Results</p> <p>The mitochondrial DNA of <it>Rhabdopleura compacta </it>corresponds in size and gene content to typical mitochondrial genomes of metazoans, but shows the strongest known strand-specific mutational bias in the nucleotide composition among deuterostomes with a very GT-rich main-coding strand. The order of the protein-coding genes in <it>R. compacta </it>is similar to that of the deuterostome ground pattern. However, the protein-coding genes have been highly affected by a strand-specific mutational pressure showing unusual codon frequency and amino acid composition. This composition caused extremely long branches in phylogenetic analyses. The unusual codon frequency points to a selection pressure on the tRNA translation system to codon-anticodon sequences of highest versatility instead of showing adaptations in anticodon sequences to the most frequent codons. Furthermore, an assignment of the codon AGG to Lysine has been detected in the mitochondrial genome of <it>R. compacta</it>, which is otherwise observed only in the mitogenomes of some arthropods. The genomes of these arthropods do not have such a strong strand-specific bias as found in <it>R. compacta </it>but possess an identical mutation in the anticodon sequence of the tRNA_Lys.</p> <p>Conclusion</p> <p>A strong reversed asymmetrical mutational constraint in the mitochondrial genome of <it>Rhabdopleura compacta </it>may have arisen by an inversion of the replication direction and adaptation to this bias in the protein sequences leading to an enigmatic mitochondrial genome. Although, phylogenetic analyses of protein coding sequences are hampered, features of the tRNA system of <it>R. compacta </it>support the monophyly of Ambulacraria. The identical reassignment of AGG to Lysine in two distinct groups may have occurred by convergent evolution in the anticodon sequence of the tRNA_Lys.</p