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Adaptations to temperature regimes in sponges: Genomic insights into the developmental and physiological evolutionary changes of early-branching metazoans

Periodic Reporting for period 1 - ADAPTOMICS (Adaptations to temperature regimes in sponges: Genomic insights into the developmental and physiological evolutionary changes of early-branching metazoans)

Reporting period: 2017-06-01 to 2019-05-31

Animals in Antarctic seas have adapted to some of the most challenging conditions found anywhere on the planet. Temperatures generally ranging between 0 to -1.8 C and a food supply which fluctuates widely from summer to winter render their survival difficult. Nevertheless, species have found the means to live in such conditions. How do they do this?

The major aim of ADAPTOMICS was the identification of the molecular mechanisms by which species can adapt to extreme environments, focusing in particular on demosponges, which are prevalent in polar seas and form the basis of Antarctic ecosystems. This allows us to begin to unravel the precise details of how species adapt to the cold, and to learn whether the same adaptive molecular mechanisms are observed in common in different species found in the same environments.

This is important for society in both specific and general ways:
- Specifically, sponges are vital components of the Antarctic benthos. By studying how they survive in these conditions, we can understand whether they will be robust to future changes in temperature. This is vital as we adjust to. and interpret the impact of, likely climate change scenarios.
- More generally, the ability to survive challenging conditions provides clues to enable us to understand how life can evolve to meet challenges. Our dataset is powerful, as it represents multiple independent evolutionary events, and will allow the examination of how reproducible evolution is.
- The resources put in place by this project will be useful for a range of future work in sponges and more generally in the investigation of Antarctic evolution.

Overall scientific objectives of this project were as follows:
Objective 1: To use transcriptomics and genomics to discover novel molecular means by which sponge species have adapted to challenging environments
Objective 2: To reveal the means of adaptation at a genetic level - whether duplication and divergence, splice variation, or other means are used to drive gene evolution
Objective 3: To determine whether these adaptations have evolved convergently in the species of sponge examined (and thus likely to be mirrored in other species in the same ecosystem) or are shared ancestrally by sponge species found in Antarctic conditions
Objective 4: To describe the role, expression and evolution of individual cold-adapted molecules in detail, both in silico and in vivo.
ADAPTOMICS was divided into 6 work packages (WP), each with specific deliverables (DL) and milestones (M).

Work Package (WP) 1: Transcriptomic analysis
Status: Fully complete. These deliverables were completed in full. A total of 9 species of demosponge were sequenced transcriptomically, with multiple samples used (DL1.1). Specific genes of interest were noted on the basis of tests for positive selection (DL1.2).

WP2: Comparative genomic analysis
Status: Fully complete, with slight modification to described work and TA. Sequencing of M. laevis and M. acerata was performed using Illumina and 10x sequencing (DL2.1). This resulted in a draft assembly of these genomic resources, which allowed both verification data derived from transcriptomic analyses (DL2.2) and raw analysis of genome content and structure (DL2.3).

WP3: Targeted gene investigation
Status: Fully complete with improvements to described work and TA. Differential gene expression was confirmed by RT PCR (DL3.1) but as the most interesting differences were qualitative rather than quantitative, this was less important than anticipated, and precise tests of selection were used (HyPhy/CODEML). An EMBO course (EMBO Popgen) was attended. This formed the basis of much further work (DL3.2). Target genes were found to be almost always ubiquitous amongst the Metazoa (DL3.3) with only a few cases limited to sponges alone.

WP4: Functional testing of target genes
Status: Fully complete, with targeted functional research. A research secondment was undertaken in the Ruiz-Trillo Lab (IBE, Barcelona). While there the fellow performed several tests regarding gene function in two species of opisthokont, one from cold waters, Sphaeroforma arctica, and a warm-water outgroup, Capsaspora owczarzaki. Instead of candidate gene tests alone, on the basis of our findings we performed tests focused on membrane fluidity and actin cytoskeletal dynamics in these species (DL4.1 4.2 TA3).

WP5: Co-ordination and management of research
Status: Fully complete. Meetings were held on a regular basis in the Riesgo lab, with informal discussion occurring on an almost daily basis (DL 5.1). Risks were managed appropriately and the project delivered efficiently (DL 5.2). A Data Management Plan was provided voluntarily (DL 5.3). The fellow attended a variety of training sessions held for postdoctoral fellows and mixed groups at the NHM (DL 5.4 TA4).

WP6: Outreach activities and the communication of results to a wider audience
Status: Fully complete. Numerous opportunities arose to communicate work directly to the general public (DL6.1) at events such as the European Researchers’ Night, Science Lates, “Science Uncovered” and more informally. To reach a more focused scientific community, a number of conferences and symposia were attended in the course of the project. 4 have been published, with more in process. Further, the fellow gave invited talks in a number of institutions, detailing his results (DL 6.2).
"The ADAPTOMICS project, over the course of the two years it ran, lead to the generation of a number of fundamental molecular resources from Antarctic sponges and related species, for the examination of adaptation to extreme environments. This knowledge specifically was used to determine whether independent lineages of demosponge have converged upon the same solutions to evolutionary problems. Our data suggests they have, especially in a suite of genes related to membrane structure, flexibility and function, as well as a number of cytoskeletal genes involved with cellular support. These targets were subjected to functional testing.

This work has lead to advances in the fields of evolution and climate adaptation. These findings will be useful as we understand the impacts of climate change on specialist species (such as the Antarctic sponges examined here). This will be useful for policy makers, as well as of interest to the general public and scientific audiences.

The project has lead to 4 publications available at the time of writing, with several other publications making their way through the review process. As part of the project, the fellow gave 11 contributed or invited talks at conferences and seminar series in the UK, Europe and North America. It also allowed the fellow to present his results to the general public at a number of formal and informal events, particularly at the Natural History Museum, London, his host institution, where he delivered ""Science Uncovered"" talks and met the public at ""Lates"" and ""European Research Night"" events.

This work lead to a number of learning and professional advancement opportunities for the fellow employed on this project. These included additional training in bioinformatic analyses, increased ‘wet lab’ experience, opportunities to teach and communicate his science, and formal training in a number of “soft skills” that allowed him to continue his professional development in a manner that will aid his future prospects in research and assist him in his career path."
Giving a presentation on the results of the project at the IBE, Barcelona