Macro-evolution in microorganisms: marine-terrestrial transitions as a case-study for adaptive radiations in bacteria

Understanding the ecological and evolutionary drivers of biodiversity is of central importance to biology. However, knowledge on the extent, tempo, mode, and drivers of bacterial diversification greatly lags behind that of animals and plants. This knowledge gap is problematic, as bacteria are fundamental to biogeochemistry and ecosystem functioning, agriculture, industry, and human health, but also because there is great intrinsic value in understanding the evolution of the most ancient and diverse group of organisms on the planet.

Adaptive radiations arguably form the best examples of the power of natural selection to generate biodiversity. These evolutionary bursts of diversification occur when a single ancestral type is faced with ecological opportunity enabling diversification into a multitude of specialised types. Unique colonisation events of virgin ecosystems, often the cause of adaptive radiations in animals and plants, are highly improbable in bacteria because of their large population sizes and high dispersal capacity. However, adaptive radiations could also be spurred by the evolution of 'key innovations' that open up new ecological opportunity (e.g. the evolution of the pharyngeal jaw allowing radiation of Rift Lake cichlids). It can be hypothesised that the extraordinary ability of bacteria to acquire novel traits via Lateral Gene Transfer (LGT) could make the evolution of key innovations and thus subsequent adaptive radiations especially prevalent. However, despite having a long history of research in multicellular organisms, it remains unknown whether adaptive radiations are an important driver in natural bacterial populations.

One of the most drastic environmental transitions for metazoans and bacteria alike is that between marine and terrestrial environments. Marine-terrestrial transitions occasionally occur in bacterial taxa and are accompanied by significant rewiring of central metabolism. These transitions thus present an excellent model for the exploration of novel adaptive zones through key innovations. We will sample the ecologically versatile Myxobacteria from a range of terrestrial and marine habitats in Cornwall, U.K. to systematically study adaptive radiations in bacteria.

First, we will estimate the frequency whereby myxobacterial lineages transition from marine to terrestrial habitats or vice versa. To do so, we will sequence a marker gene in replicated environmental samples to build a high-resolution evolutionary tree on which habitat preferences of lineages are mapped. Second, we hypothesise that lineages that colonise new habitats undergo adaptive radiations, leaving an imprint of increased branching rate in the phylogenetic tree compared to lineages that remain in their ancestral habitat. Third, we will retrieve genomes through isolate-based genome sequencing and by assembling genomes from metagenomes to identify the key adaptation(s) underlying marine-terrestrial transitions, elucidate whether they are the result of LGT events, and to explore the genomic consequences of a transition and subsequent radiation.

There is a rich tradition of studying adaptive radiations in eukaryotes. Although theory and empirical data suggest that bacteria could likewise experience bursts of adaptive evolution, this will be the first largescale, purpose-designed analysis of adaptive radiations in bacteria. Results generated in this pioneering project will pave the way for studies in other bacterial taxa colonising different environments through different mechanisms and more generally provide impetus for the detailed study of macro-evolutionary patterns generating prokaryote diversity which ultimately underlies the functioning of all ecosystems.

This proposal focuses on fundamental questions in evolutionary biology. As such, the results generated are expected to directly impact on the scientific community (see Academic Beneficiaries). Understanding the ecological drivers of bacterial diversification ultimately informs the manipulation of bacteria in agriculture, industry and healthcare as well as in ecosystem management. With regards to this research proposal we have investigated opportunities for short- and medium-term impact within aforementioned industrial sectors, however, no immediate applied, economic or social benefits are likely to be associated with this research. We will however engage with the general public through activities in the Eden project in Cornwall to generate societal impact (see 'Pathways to Impact').