An understanding of ctenophore biology is critical for reconstructing events that occurred early in animal evolution. Towards this goal, we have sequenced, assembled, and annotated the genome of the ctenophore Mnemiopsis leidyi. Our phylogenomic analyses of both amino acid positions and gene content suggests that ctenophores rather than sponges are the sister lineage to all other animals. Mnemiopsis lacks many of the genes found in bilaterian mesodermal cell types, suggesting that these cell types evolved independently. The set of neural genes in Mnemiopsis is similar to that of sponges, indicating that sponges may have lost a nervous system. These results present a new view of early animal evolution that accounts for major losses and/or gains of sophisticated cell types, including nerve and muscle cells.

Placozoans are a phylum of nonbilaterian marine animals currently represented by a single described species, Trichoplax adhaerens, Schulze 1883. Placozoans arguably show the simplest animal morphology, which is identical among isolates collected worldwide, despite an apparently sizeable genetic diversity within the phylum. Here, we use a comparative genomics approach for a deeper appreciation of the structure and causes of the deeply diverging lineages in the Placozoa. We generated a high-quality draft genome of the genetic lineage H13 isolated from Hong Kong and compared it to the distantly related T. adhaerens. We uncovered substantial structural differences between the two genomes that point to a deep genomic separation and provide support that adaptation by gene duplication is likely a crucial mechanism in placozoan speciation. We further provide genetic evidence for reproductively isolated species and suggest a genus-level difference of H13 to T. adhaerens, justifying the designation of H13 as a new species, Hoilungia hongkongensis nov. gen., nov. spec., now the second described placozoan species and the first in a new genus. Our multilevel comparative genomics approach is, therefore, likely to prove valuable for species distinctions in other cryptic microscopic animal groups that lack diagnostic morphological characters, such as some nematodes, copepods, rotifers, or mites.

Sponges and evolutionary origins Sponges represent our distant animal relatives. They do not have a nervous system but do have a simple body for filter feeding. Surveying the cell types in the freshwater sponge Spongilla lacustris , Musser et al . found that many genes important in synaptic communication are expressed in cells of the small digestive chambers. They found secretory machinery characteristic of the presynapse in small multipolar cells contacting all other cells and also the receptive apparatus of the postsynapse in the choanocytes that generate water flow and digest microbial food. These results suggest that the first directed communication in animals may have evolved to regulate feeding, serving as a starting point on the long path toward nervous system evolution. —BAP

Animals have a carefully orchestrated relationship with oxygen. When exposed to low environmental oxygen concentrations, and during periods of increased energy expenditure, animals maintain cellular oxygen homeostasis by enhancing internal oxygen delivery, and by enabling the anaerobic production of ATP. These low-oxygen responses are thought to be controlled universally across animals by the hypoxia-inducible factor (HIF). We find, however, that sponge and ctenophore genomes lack key components of the HIF pathway. Since sponges and ctenophores are likely sister to all remaining animal phyla, the last common ancestor of extant animals likely lacked the HIF pathway as well. Laboratory experiments show that the marine sponge Tethya wilhelma maintains normal transcription under oxygen levels down to 0.25% of modern atmospheric saturation, the lowest levels we investigated, consistent with the predicted absence of HIF or any other HIF-like pathway. Thus, the last common ancestor of all living animals could have metabolized aerobically under very low environmental oxygen concentrations.

Scientific drilling has identified a biosphere in marine sediments , which contain many uncultivated microbial groups known only by their DNA sequences . Recycling of organic matter in sediments is an important component of biogeochemical cycles because marine sediments are critical for long-term carbon storage . Turnover of carbon is hypothesized to be driven by the secretion of enzymes by microbial organisms , which act to break down macromolecules into constitutive monomers that can be transported into cells. As such, the nature of the microbial secretome often influences the function of a community . However, the microbial groups involved in this process and the biochemistry they encode is poorly understood. Here, we show that expressed genes from 5 to 159 meters below the seafloor (mbsf) encode numerous candidate peptidases and carbohydrate-active enzymes ('CAZymes') targeted for secretion. The majority (90-99%) were assigned to Bacteria, of which 12% shared the highest sequence similarity with candidate phyla . The remaining putatively secreted proteins shared highest sequence similarity with archaeal and fungal enzymes, which peak in two redox transition zones . In the shallower redox zone at 30 mbsf, 20% of the transcripts encoding putative secreted peptidases were assigned to lineages of uncultivated Archaea. The target compounds of the predicted secreted proteome show a preference for necromass in the form of microbial cell envelopes as well as plankton and algal detritus. The predicted fungal secreted proteome encodes CAZymes not present in the predicted bacterial or archaeal secreted proteomes, indicating that fungi putatively play a minimal but specialized role in subseafloor carbohydrate recycling.