Global distribution, diversity hot spots and niche transitions of an astaxanthin‐producing eukaryotic microbe

Abstract

Microbes establish very diverse but still poorly understood associations with other microscopic or macroscopic organisms that do not follow the more conventional modes of competition or mutualism. Phaffia rhodozyma, an orange-coloured yeast that produces the biotechnologically relevant carotenoid astaxanthin, exhibits a Holarctic association with birch trees in temperate forests that contrasts with the more recent finding of a South American population associated with Nothofagus (southern beech) and with stromata of its biotrophic fungal parasite Cyttaria spp. We investigated whether the association of Phaffia with Nothofagus-Cyttaria could be expanded to Australasia, the other region of the world where Nothofagus are endemic, studied the genetic structure of populations representing the known worldwide distribution of Phaffia and analysed the evolution of the association with tree hosts. The phylogenetic analysis revealed that Phaffia diversity in Australasia is much higher than in other regions of the globe and that two endemic and markedly divergent lineages seem to represent new species. The observed genetic diversity correlates with host tree genera rather than with geography, which suggests that adaptation to the different niches is driving population structure in this yeast. The high genetic diversity and endemism in Australasia indicate that the genus evolved in this region and that the association with Nothofagus is the ancestral tree association. Estimates of the divergence times of Phaffia lineages point to splits that are much more recent than the break-up of Gondwana, supporting that long-distance dispersal rather than vicariance is responsible for observed distribution of P. rhodozyma.

12 Tremellomycetes and Related Groups

“…Bullera alba is frequently isolated from the phylloplane (Sampaio 2004). Xanthophyllomyces dendrorhous is known from the sap of various tree species (David-Palma et al 2014;. Some species of Fellomyces have only been found on lichen thalli (Lopandic et al 2011).…”

Comparative genomics provides new insights into the diversity, physiology, and sexuality of the only industrially exploited tremellomycete: Phaffia rhodozyma

“…This exceptional property of P. rhodozyma is supposed to have evolved as a result of its adaptation to live in association with plant substrates, particularly tree exudates in mountain environments where ROS are generated by high levels of UV radiation (UVR) [5], and/or the phylloplane of mountain trees where cells are directly affected by UV radiation [6, 7]. In line with this hypothesis, additional photoprotective strategies were found in P. rhodozyma , such as the synthesis of an antioxidant compound named Phaffiol [8] and the accumulation of mycosporine-glutaminol-glucoside (MGG), a UVB-screening compound that also has antioxidant properties [9, 10].…”

“…in the Southern Hemisphere [6, 7, 14]. Many genetically distinct, natural populations of P. rhodozyma are known worldwide, but most of the diversity is found in the Southern Hemisphere, mainly in Australasia, whereas Holarctic populations are mostly genetically uniform [6].…”

“…in the Southern Hemisphere [6, 7, 14]. Many genetically distinct, natural populations of P. rhodozyma are known worldwide, but most of the diversity is found in the Southern Hemisphere, mainly in Australasia, whereas Holarctic populations are mostly genetically uniform [6]. The population structure of this yeast seems to be driven by adaptation to the different niches as a result of long-distance dispersal, and the observed genetic diversity correlates with host tree genera, rather than with geography [6].…”

“…It was later determined that both strains belong to the same species [19], a confusion resulting from the fact that the anamorphic strain CBS 5905 is a hybrid or admixed strain derived from two genetically distinct lineages of P. rhodozyma [6]. Thus, we consider the Holarctic strain CBS 7918 T to be the valid type strain for the species.…”