CR2025_56 Molecular ecology of seagrass associated meiofauna, in healthy, declining, and restored meadows

Lead Supervisor: Christopher Laumer, Natural History Museum

Email: Christopher.laumer1@nhm.ac.uk

Co-supervisors: Richard Unsworth, Department of Biosciences, Swansea University

The meiofauna are communities of microscopic invertebrates and protists too small to be retained on a 1 mm sieve, exemplified by the hyperdiverse and unique organisms whose life cycles are carried out entirely in the interstitial spaces of marine sediments (Laumer, 2024) – encompassing nematodes, copepods, flatworms, tardigrades, and many other groups (indeed, 2/3 of animal phyla). They show high potential as ecological indicators, with up to 10s to >100 species co-occurring per litre of sediment, and high beta-diversity across samples, being controlled by variables such as organic inputs, granulometry, and dissolved oxygen. Because these communities can be so diverse, they also include a range of more generalist, readily dispersive, and specialist species that are slow to recolonize after ecological disruption.

In marine systems, seagrass (e.g. Zostera, Poseidonia) meadows are known as sites of great ecological importance owing to their role as nurseries for many fish species and macroinvertebrates, and due to their role as “blue” carbon sinks from burial of seagrass primary production (Unsworth et al., 2024). Seagrasses can also harbour particularly interesting and diverse meiofauna (García-Gómez et al., 2022), especially those associated to sediments showing an oxygen-sulfide gradient, with representation of rare lineages such as Gnathostomulida or Solenofilomorphidae, and examples of remarkable chemolithoautotrophic bacteria living in symbiosis with meiobenthic hosts, such as the flatworm Paracatenula (Gruber-Vodicka et al., 2011), the gutless oligochaete Olavius (Dubilier et al., 2001), or the bacteria-covered Stilbonematinae (Scharhauser et al., 2024). Seagrass associated meiofauna probably play important ecological roles, not least in improving oxygenation of sulfide-rich sediments through bioturbation (Bonaglia et al., 2020).

Unfortunately, seagrass meadows have been threatened by human activities associated to coastal development, discharge of sewage and agricultural runoff, and climate change; in the UK, historical evidence indicates loss of between 44-92% of seagrass meadows since the industrial revolution (Green et al., 2021). However, seagrasses are resilient, and when anthropogenic pressures are relieved, these important ecosystems have astonishing potential to regenerate, especially when aided by conservation activities such as seed-planting. The roles that seagrass-associated meiofauna play in ecosystem decline and regeneration, however, remain unclear; a question of particular interest is whether the meiofauna should also be specifically targeted or “re-seeded” from an ecologically healthy area in conservation interventions, not least given the low intrinsic dispersal potential of some members of these communities.

In this project, you will use cutting-edge genomics techniques such as transcriptome skimming, metagenomics, and metabarcoding, all carried out on the Oxford Nanopore long-read sequencing platform, to profile seagrass-associated meiofauna communities. There will be a strong emphasis on populating reference databases with “DNA barcode” loci from individually isolated exemplar specimens collected in representative UK seagrass meadows, since prior studies have shown that this is crucial to being able to interpret data from bulk-sequencing techniques such as metabarcoding (Cowart et al., 2015; Macher et al., 2024). In the Laumer lab at the NHM, we are routinely mining such data from de novo transcriptome assemblies made from shallowly sequenced libraries (ca. 50,000-100,000 reads/specimen), a cost-effective approach we term transcriptome skimming. You will have opportunities to work in the classical mode, morphologically identifying 100s of individual species via differential interference contrast microscopy and digital UHD video vouchering. We will also explore high-throughput “reverse taxonomy” approaches (Markmann and Tautz, 2005) to transcriptome skim 10,000s of specimens for which we will forgo microscopical examination, relying instead on automated phylogenetic placement and species delimitation algorithms for provisional species identification.

Building on the databases you will help to populate in the early years of your PhD, we will then explore the potential of metabarcoding and/or metagenomic sequencing to cheaply and quickly profile entire communities from quantitative sediment samples. Building on a network of established seagrass meadow sites under regular monitoring in the Unsworth lab, including sites currently being restored via Project Seagrass, we will collect samples across environmental gradients and under varying levels of anthropogenic pressure – the core aim being to quantify community overlap between environmentally similar but geographically disjunct meadows, and identify community members enriched in ecologically healthy meadows. Opportunities to explore specific meiofaunal ecological interactions, e.g. seed-associated nematodes or with protistan seagrass parasites, may also be considered. Such research will be important to adding a meiofaunal perspective to the global efforts to conserve and rewild these iconic habitats.

Training opportunities: 

The Laumer lab regularly (~6 weeks/year) undertakes fieldwork domestically within the UK and internationally, to sample meiobenthic communities; the student would be invited to join several such expeditions during their study. We expect you would also work closely with Project Seagrass, a charity whose mission is to document the health of seagrass meadows and “rewild” in areas where seagrasses have historically flourished. 

Student profile: 

We are looking for candidates to have or expecting to receive a first or upper-second class honours degree and a Master’s degree in an area relevant to the project such as marine biology, zoology, biodiversity and conservation, evolutionary ecology, systematics, taxonomy, molecular evolution, or bioinformatics. Candidates must also have experience conducting research in a laboratory environment, whether dry or wet lab. Knowledge of phylogenetics, high-performance computing, microscopy, python and R programming, would be highly advantageous but are not required. SCUBA diving qualifications and prior experience in fieldwork, especially in a marine context, would be valuable. 

Please note: Due to the nature of this project and to comply with visa regulations, only Home students should apply.

Co-Sponsorship details:

This project will be looking to apply for a CASE award with Project Seagrass.

References:

• Bonaglia, S., Hedberg, J., Marzocchi, U., Iburg, S., Glud, R.N., Nascimento, F.J.A., 2020. Meiofauna improve oxygenation and accelerate sulfide removal in the seasonally hypoxic seabed. Environ. Res. 159, 104968. https://doi.org/10.1016/j.marenvres.2020.104968
• Cowart, D.A., Pinheiro, M., Mouchel, O., Maguer, M., Grall, J., Miné, J., Arnaud-Haond, S., 2015. Metabarcoding Is Powerful yet Still Blind: A Comparative Analysis of Morphological and Molecular Surveys of Seagrass Communities. PLOS ONE 10, e0117562. https://doi.org/10.1371/journal.pone.0117562
• Dubilier, N., Mülders, C., Ferdelman, T., de Beer, D., Pernthaler, A., Klein, M., Wagner, M., Erséus, C., Thiermann, F., Krieger, J., Giere, O., Amann, R., 2001. Endosymbiotic sulphate-reducing and sulphide-oxidizing bacteria in an oligochaete worm. Nature 411, 298–302. https://doi.org/10.1038/35077067
• García-Gómez, G., García-Herrero, Á., Sánchez, N., Pardos, F., Izquierdo-Muñoz, A., Fontaneto, D., Martínez, A., 2022. Meiofauna is an important, yet often overlooked, component of biodiversity in the ecosystem formed by. Invertebr. Biol. 141, e12377. https://doi.org/10.1111/ivb.12377
• Green, A.E., Unsworth, R.K.F., Chadwick, M.A., Jones, P.J.S., 2021. Historical Analysis Exposes Catastrophic Seagrass Loss for the United Kingdom. Front. Plant Sci. 12. https://doi.org/10.3389/fpls.2021.629962
• Gruber-Vodicka, H.R., Dirks, U., Leisch, N., Baranyi, C., Stoecker, K., Bulgheresi, S., Heindl, N.R., Horn, M., Lott, C., Loy, A., Wagner, M., Ott, J., 2011. Paracatenula, an ancient symbiosis between thiotrophic Alphaproteobacteria and catenulid flatworms. Proc. Natl. Acad. Sci. 108, 12078–12083. https://doi.org/10.1073/pnas.1105347108
• Laumer, C., 2024. Meiofauna. Curr. Biol. 34, R223–R225. https://doi.org/10.1016/j.cub.2024.02.017
• Macher, J.-N., Martínez, A., Çakir, S., Cholley, P.-E., Christoforou, E., Curini Galletti, M., van Galen, L., García-Cobo, M., Jondelius, U., de Jong, D., Leasi, F., Lemke, M., Rubio Lopez, I., Sánchez, N., Sørensen, M.V., Todaro, M.A., Renema, W., Fontaneto, D., 2024. Enhancing metabarcoding efficiency and ecological insights through integrated taxonomy and DNA reference barcoding: A case study on beach meiofauna. Ecol. Resour. 24, e13997. https://doi.org/10.1111/1755-0998.13997
• Markmann, M., Tautz, D., 2005. Reverse taxonomy: an approach towards determining the diversity of meiobenthic organisms based on ribosomal RNA signature sequences. Philos. Trans. R. Soc. B Biol. Sci. 360, 1917–1924. https://doi.org/10.1098/rstb.2005.1723
• Scharhauser, F., Saavedra, D.E.M., Pröts, P., Ott, J.A., Geier, B., Gruber-Vodicka, H.R., Polikarpov, M., Bourenkov, G., Leisch, N., 2024. Revision of the genus Robbea (Stilbonematinae: Desmodoridae), worldwide abundant marine nematodes with chromophoric Fe–Br inclusions and the description of a new stilbonematine genus. Zool. J. Linn. Soc. zlae005. https://doi.org/10.1093/zoolinnean/zlae005
• Unsworth, R.K.F., Jones, B.L.H., Bertelli, C.M., Coals, L., Cullen-Unsworth, L.C., Mendzil, A.F., Rees, S.C., Taylor, F., Walter, B., Evans, A.J., 2024. Ten golden rules for restoration to secure resilient and just seagrass social-ecological systems. Plants People Planet 6, 587–603. https://doi.org/10.1002/ppp3.10560