The evolution of globally occurring microorganisms is highly driven by dispersal and speciation in isolation

Many microorganism species can be found all across the globe. Their seemingly global distributions have long caused a debate whether microorganisms can disperse very easily and geographic barriers have any effect on them, or whether it has taken them a long time to get everywhere.
Trying to answer that question, a new large-scale genetic study in Nature Communications revealed how a single-celled alga has spread across the globe and in its journey radiated into an unprecedented species diversity since the Eocene/Oligocene global cooling period. In contrast to previous beliefs, it hereby shows that the evolution of microorganisms is highly driven by colonisation to suitable habitats and subsequent speciation in isolation. Although this has long been recognised as a driving force for speciation in larger organisms, it is now also shown to be an important force for speciation in microbial species.

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Microbial biogeography: putting the distribution of a global microbe on the map
 
Many microbial species, i.e. protists, bacteria, archaea and fungi, often have very similar appearances in various corners of the globe. It is therefore generally thought that they lack the biogeographic structure and the clear speciation patterns found in larger organisms. Instead, their supposedly high dispersal rates and large population sizes have long led to the assumption that many microorganisms have global geographic distributions. 
To investigate this, Pinseel et al. (2020) studied the evolutionary history of a globally occurring terrestrial diatom species, Pinnularia borealis - a small type of single-celled algae living in terrestrial habitats such as soils and mosses. Sampling >1500 environmental samples across the globe containing >800 strains, the study looked into morphological and genetic analyses to study the species’ evolutionary history, and the timescale on which this small diatom managed to cover most of the planet’s far-flung corners of the globe.

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​Similar appearance, yet many species
 
The global dataset revealed an unexpected high level of genetic species-diversity: while the strains were very similar in morphological appearance, surprisingly, >120 genetically differentiated species could be found. This suggests that,  What has previously been thought of as a globally occurring species, in fact is a so-called “species complex”, i.e. a group of closely related organisms that are similar in appearance, however composed of genetically distinguishable species. 

​Geographic isolation shaping diversity patterns
 
The study found that diversification was largely driven by dispersal of new geographic areas, and subsequent evolution in the resulting isolated populations. This might not be so surprising, as we have long known this mechanism to be an important driver for evolution in larger organisms (e.g. in the famous example of Darwin’s finches), yet it is contrasting to the long-held view of ‘global’ geographic distributions of many microscopic species. 

Automated species delimitation methods showed a large diversity of species in what was thought to be just one species.

​The analyses, however, also suggested that, despite P. borealis being a small, microscopic algae, has been quite good at dispersing. For example, the analyses revealed that all continents had been colonised multiple independent times. In particular, it was surprising that the sub-Antarctic and Antarctic, though highly isolated places, were colonised at least eight independent times, and in several cases through long-distance dispersal from the Northern Hemisphere.

​Timing of species diversification and the transition to open terrestrial habitats 
 
Luckily, diatoms have a very good fossil record, and species diversity can be quite accurately calculated over time. Using fossil evidence and genetic dating techniques the radiation of the diatom across the globe was found to have originated since the Eocene/Oligocene boundary (25.0–36.1 million years ago). This period was characterised by a profound change in climate, as the Earth shifted from a greenhouse to an icehouse state, and known as a time of large-scale extinction and floral and faunal turnover. The period, associated with colder and drier climates, also marks the onset of a global expansion of open terrestrial landscapes, in which P. borealis currently thrives. 

Time-calibrated species tree of the P. borealis complex. Coloured bars next to the phylogeny indicate the biogeographic region(s) of each species: dark blue: Arctic zone; light blue: boreal zone; purple North America (excl. Arctic); grey: Madagascar; pink: South America; orange: Australasia; yellow: sub-Antarctic; dark red: Antarctic. In the middle-left: species accumulation curve showing the sample-based interpolation (rarefaction) and extrapolation of the P. borealis species delimited in this study. Below: raw (blue) and smoothed (black) oxygen-isotope data reflecting changes in global temperature and continental ice-sheet volume, overlaid with a "lineage-through-time plot" (semi-logarithmic scale) of the P. borealis complex.

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​How many times would one need to sample to get all extant diversity?
 
Indeed, despite that over 1500 samples were obtained, the large global sampling effort was still not nearly enough to capture al the diversity within P. borealis. Extrapolation analyses, investigating how the number of species increases with the number of added samples, suggested that that nearly ten thousand environmental samples would need to be gathered all across the globe to find the majority of lineages of just this species complex alone. This means that, at that point one will likely have found most of the global diversity that exists within P. borealis, which was estimated to equal about 415 species. This species diversity far exceeded previous estimates for a diatom lineage of this age (since the Eocene/Oligocene boundary). The high diversity within this species complex alone reflects the likely hidden diversity of other groups of the ‘rare biosphere’.

​Implications for general understanding of drivers shaping microbial biogeography 
 
All in all, the new study reveals how ‘rare biosphere’ taxa, which are key players in the global carbon and nutrient cycles, are composed of astonishingly high levels of diversity across the globe. It reveals, contrary to long-held views, how dispersal and subsequent evolution in isolation plays a large role in the evolution of small micro-organisms. The evolutionary history of this one, seemingly insignificant, microscopic algae, illuminates the hidden diversity within the world of small microscopic life, which we still know so little about.


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For more information see:
Pinseel, E., Janssens, S.B., Verleyen, E., Vanormelingen, P., Kohler, T.J., Biersma, E.M., Sabbe, K., Van de Vijver, B. & Vyverman, W. (2020) Global radiation in a rare biosphere soil diatom. Nature Communications 11, 2382. https://doi.org/10.1038/s41467-020-16181-0