Ecological niche differentiation in soil cyanobacterial communities across the globe

Abstract Cyanobacteria are key organisms in the evolution of life on Earth, but their distribution and environmental preferences in terrestrial ecosystems remain poorly understood. This lack of knowledge is particularly evident for two recently discovered non-photosynthetic cyanobacterial classes, Melainabacteria and Sericytochromatia, limiting our capacity to predict how these organisms and the important ecosystem functions they perform will respond to ongoing global change. Here, we conducted a global field survey covering a wide range of vegetation types and climatic conditions to identify the environmental factors associated with the distribution of soil cyanobacterial communities. Network analyses revealed three major clusters of cyanobacterial phylotypes, each one dominated by members of one of the extant classes of Cyanobacteria (Oxyphotobacteria, Melainabacteria and Sericytochromatia), suggesting that species within these taxonomic groups share similar environmental preferences. Melainabacteria appear mostly in acidic and humid ecosystems, especially forests, Oxyphotobacteria are prevalent in arid and semiarid areas, and Sericytochromatia are common in hyperarid oligotrophic environments. We used this information to construct a global atlas of soil cyanobacteria. Our results provide novel insights into the ecology and biogeography of soil cyanobacteria and highlight how their global distribution could change in response to increased aridity, a landmark feature of climate change in terrestrial ecosystems worldwide. Significance statement Cyanobacteria have shaped the history of life on Earth and can be important photosynthesizers and nitrogen fixers in terrestrial ecosystems worldwide. The recent discovery of two non-photosynthetic classes has advanced our understanding of their evolution, but their distribution and environmental preferences remain poorly described. Using a global survey conducted across 237 locations on six continents, we identified three main groups of soil cyanobacteria with contrasting environmental preferences: acidic and humid ecosystems, arid and semiarid areas, and hyperarid oligotrophic ecosystems. We then constructed the first global atlas of soil cyanobacteria, an important advance in our understanding of the ecology and biogeography of these functionally important organisms.