Rapid Evolutionary Rates and Unique Genomic Signatures Discovered in the First Reference Genome for the Southern Ocean Salp,Salpa thompsoni(Urochordata, Thaliacea)

Abstract

A preliminary genome sequence has been assembled for the Southern Ocean salp, Salpa thompsoni (Urochordata, Thaliacea). Despite the ecological importance of this species in Antarctic pelagic food webs and its potential role as an indicator of changing Southern Ocean ecosystems in response to climate change, no genomic resources are available for S. thompsoni or any closely related urochordate species. Using a multiple-platform, multiple-individual approach, we have produced a 318,767,936-bp genome sequence, covering >50% of the estimated 602 Mb (±173 Mb) genome size for S. thompsoni. Using a nonredundant set of predicted proteins, >50% (16,823) of sequences showed significant homology to known proteins and ∼38% (12,151) of the total protein predictions were associated with Gene Ontology functional information. We have generated 109,958 SNP variant and 9,782 indel predictions for this species, serving as a resource for future phylogenomic and population genetic studies. Comparing the salp genome to available assemblies for four other urochordates, Botryllus schlosseri, Ciona intestinalis, Ciona savignyi and Oikopleura dioica, we found that S. thompsoni shares the previously estimated rapid rates of evolution for these species. High mutation rates are thus independent of genome size, suggesting that rates of evolution >1.5 times that observed for vertebrates are a broad taxonomic characteristic of urochordates. Tests for positive selection implemented in PAML revealed a small number of genes with sites undergoing rapid evolution, including genes involved in ribosome biogenesis and metabolic and immune process that may be reflective of both adaptation to polar, planktonic environments as well as the complex life history of the salps. Finally, we performed an initial survey of small RNAs, revealing the presence of known, conserved miRNAs, as well as novel miRNA genes; unique piRNAs; and mature miRNA signatures for varying developmental stages. Collectively, these resources provide a genomic foundation supporting S. thompsoni as a model species for further examination of the exceptional rates and patterns of genomic evolution shown by urochordates. Additionally, genomic data will allow for the development of molecular indicators of key life history events and processes and afford new understandings and predictions of impacts of climate change on this key species of Antarctic pelagic ecosystems.

Population Genomics of Marine Zooplankton

“…Published genomic resources: It can be argued that there are no universally-accepted model species among the marine zooplankton; in many cases, there are no closely-related model organisms to which extrapolations or comparisons can be made (Ellegren 2014). However, the number of marine zooplankton species targeted for genome-scale studies is growing, including species ranging phylogenetically from the Cnidaria to the Urochordata and including ecologically-important or keystone species for some pelagic ecosystems, such as the Southern Ocean salp, Salpa thompsoni (Jue et al 2016) ( Table 1). …”

“…Notably, all the reference genomes available are from organisms whose genome size estimates are significantly smaller than 1GB, presumably since the depth of coverage required is low enough to represent a feasible investment of resources in terms of fiscal and computational effort. While reference quality assemblies are ideal (e.g., Oikopleura dioica, Denoeud et al 2010), lower coverage assemblies can still provide a high enough N50-value (i.e., the weighted median statistic such that 50% of the entire assembly is contained in contigs or scaffolds equal to or larger than this value) to afford extensive gene predictions (e.g., Jue et al 2016).…”

“…Another recent study (Jue et al 2016) produced a preliminary reference genome for the species, identified more than 50% of sequences, and generated both SNP variant and INDEL predictions as a resource for future phylogenetic and population studies.…”

“…An initial survey of small RNAs revealed the presence of known, conserved miRNAs, novel miRNA genes, and unique piRNA for various developmental stages (Jue et al 2016), suggesting possible genomic bases of the successful adaptation of the species to the changing climate of the Southern Ocean.…”

“…For instance, sequencing of the salp genome revealed novel miRNA genes and unique piRNAs (Jue et al 2016), while the genome of Pacific sea gooseberry, Pleurobrachia bachei, is apparently lacking the canonical miRNA machinery and HOX genes (Moroz et al 2014). …”