Turnover of Lecanoroid Mycobionts and Their Trebouxia Photobionts Along an Elevation Gradient in Bolivia Highlights the Role of Environment in Structuring the Lichen Symbiosis.

Ian D Medeiros,Carlos J Pardo-De La Hoz,Jolanta Miadlikowska,Adam Flakus,Pamela Rodriguez-Flakus,François Lutzoni,Lucyna Śliwa,Edyta Mazur,Elżbieta Cieślak

doi:10.3389/fmicb.2021.774839

Ian D Medeiros, Carlos J Pardo-De La Hoz + Show 7 more

Open Access

https://doi.org/10.3389/fmicb.2021.774839

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Abstract

Shifts in climate along elevation gradients structure mycobiont–photobiont associations in lichens. We obtained mycobiont (lecanoroid Lecanoraceae) and photobiont (Trebouxia alga) DNA sequences from 89 lichen thalli collected in Bolivia from a ca. 4,700 m elevation gradient encompassing diverse natural communities and environmental conditions. The molecular dataset included six mycobiont loci (ITS, nrLSU, mtSSU, RPB1, RPB2, and MCM7) and two photobiont loci (ITS, rbcL); we designed new primers to amplify Lecanoraceae RPB1 and RPB2 with a nested PCR approach. Mycobionts belonged to Lecanora s.lat., Bryonora, Myriolecis, Protoparmeliopsis, the “Lecanora” polytropa group, and the “L.” saligna group. All of these clades except for Lecanora s.lat. occurred only at high elevation. No single species of Lecanoraceae was present along the entire elevation gradient, and individual clades were restricted to a subset of the gradient. Most Lecanoraceae samples represent species which have not previously been sequenced. Trebouxia clade C, which has not previously been recorded in association with species of Lecanoraceae, predominates at low- to mid-elevation sites. Photobionts from Trebouxia clade I occur at the upper extent of mid-elevation forest and at some open, high-elevation sites, while Trebouxia clades A and S dominate open habitats at high elevation. We did not find Trebouxia clade D. Several putative new species were found in Trebouxia clades A, C, and I. These included one putative species in clade A associated with Myriolecis species growing on limestone at high elevation and a novel lineage sister to the rest of clade C associated with Lecanora on bark in low-elevation grassland. Three different kinds of photobiont switching were observed, with certain mycobiont species associating with Trebouxia from different major clades, species within a major clade, or haplotypes within a species. Lecanoraceae mycobionts and Trebouxia photobionts exhibit species turnover along the elevation gradient, but with each partner having a different elevation threshold at which the community shifts completely. A phylogenetically defined sampling of a single diverse family of lichen-forming fungi may be sufficient to document regional patterns of Trebouxia diversity and distribution.

Highlights

Alexander von Humboldt’s Essai sur La Géographie des Plantes was revolutionary for biogeography (Schrodt et al, 2019), but, with respect to lichens, Humboldt was limited by the nascent state of lichenology in the early 19th century
Phylogenetic studies of Lecanoraceae have long been bedeviled by a poorly supported backbone (Grube et al, 2004; PérezOrtega et al, 2010; Zhao et al, 2016; Yakovchenko et al, 2019; Davydov et al, 2021). Most of these studies, including recent publications, have used ITS and mtSSU to infer the phylogeny of Lecanoraceae, but those loci are most useful for resolving relationships within genera or species groups and cannot resolve deeper relationships across the entire family
The new primers and nested PCR protocols we describe in this paper can be used to sequence RPB1 and RPB2 even from extractions with a very small quantity of DNA

Summary

Introduction

Alexander von Humboldt’s Essai sur La Géographie des Plantes was revolutionary for biogeography (Schrodt et al, 2019), but, with respect to lichens, Humboldt was limited by the nascent state of lichenology in the early 19th century. There is turnover in lichenized fungi along elevation gradients, including those in the northern Andes (Wolf, 1993; Soto-Medina et al, 2019) that inspired Humboldt’s work. The mycobiont–photobiont interaction that defines the lichen symbiosis is affected by environmental conditions at micro and macro scales (e.g., James and Henssen, 1976; Peksa and Škaloud, 2011; Singh et al, 2017). What appears externally as the same lichen may represent a mycobiont species occurring with different photobiont species at different points in its range (Werth and Sork, 2014; Dal Grande et al, 2018)

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