Global patterns and rates of habitat transitions across the eukaryotic tree of life

Abstract

The successful colonization of new habitats has played a fundamental role during the evolution of life. Salinity is one of the strongest barriers for organisms to cross, which has resulted in the evolution of distinct marine and non-marine (including both freshwater and soil) communities. Although microbes represent by far the vast majority of eukaryote diversity, the role of the salt barrier in shaping the diversity across the eukaryotic tree is poorly known. Traditional views suggest rare and ancient marine/non-marine transitions but this view is being challenged by the discovery of several recently transitioned lineages. Here, we investigate habitat evolution across the tree of eukaryotes using a unique set of taxon-rich phylogenies inferred from a combination of long-read and short-read environmental metabarcoding data spanning the ribosomal DNA operon. Our results show that, overall, marine and non-marine microbial communities are phylogenetically distinct but transitions have occurred in both directions in almost all major eukaryotic lineages, with hundreds of transition events detected. Some groups have experienced relatively high rates of transitions, most notably fungi for which crossing the salt barrier has probably been an important aspect of their successful diversification. At the deepest phylogenetic levels, ancestral habitat reconstruction analyses suggest that eukaryotes may have first evolved in non-marine habitats and that the two largest known eukaryotic assemblages (TSAR and Amorphea) arose in different habitats. Overall, our findings indicate that the salt barrier has played an important role during eukaryote evolution and provide a global perspective on habitat transitions in this domain of life.

Towards all-inclusive community ecology via DNA metabarcoding

“…Recently, long-read metabarcoding has been proposed to overcome the limited resolution of many generalist primers (Jamy et al, 2022). With this approach, a very long (e.g.…”

“…With this approach, a very long (e.g. 4500 bp) DNA fragment is amplified with universal primers and then processed through technologies that allow the sequencing of long reads (Jamy et al, 2022). The long-read metabarcoding provides unprecedented taxonomic resolution compared to traditional generalist primers, still poses major technical issues (e.g.…”

Cell size is a key ecological trait associated with biogeographic patterns of microbial eukaryotes in coastal waters

“…In particular, the Pear River Estuary harbors typical coastal waters, which exhibit large environmental gradients within a small geographical area. For example, salinity is one of the strongest barriers for organisms within the eukaryotic tree of life to cross (Jamy et al, 2022). This likely explains the big changes in biogeographic patterns of microbial eukaryotes that occur in the coastal waters.…”

Who are the marine fungi?

“…This includes improved insight into terrestrial and freshwater‐to‐marine transition events, which are critical in determining marine fungal evolutionary history and contemporary diversity. Compared to other microbial eukaryotes, terrestrial/freshwater to marine transition events have occurred many more times with fungi and often only ‘recently’ in an evolutionary sense (Jamy et al, 2022 ). Why and how did these transition events specifically occur in the fungi?…”

“…The how is likely, in part, related to the incredible adaptive capabilities of fungi underpinning their ability to conquer distinct niches and general resilience/plasticity. An impact of these rapid and recent transitions to marine is that there is not much change in the phylogenetic marker genes currently used (Jamy et al, 2022 ). This could account for why many marine fungi in short read metabarcode studies appear the same or similar to terrestrial/freshwater fungi.…”