Complex Interaction Networks Among Cyanolichens of a Tropical Biodiversity Hotspot.

Ulla Kaasalainen,Veera Tuovinen,Petri Pellikka,Geoffrey Mwachala,Jouko Rikkinen

doi:10.3389/fmicb.2021.672333

Abstract

Interactions within lichen communities include, in addition to close mutualistic associations between the main partners of specific lichen symbioses, also more elusive relationships between members of a wider symbiotic community. Here, we analyze association patterns of cyanolichen symbionts in the tropical montane forests of Taita Hills, southern Kenya, which is part of the Eastern Afromontane biodiversity hotspot. The cyanolichen specimens analyzed represent 74 mycobiont taxa within the order Peltigerales (Ascomycota), associating with 115 different variants of the photobionts genus Nostoc (Cyanobacteria). Our analysis demonstrates wide sharing of photobionts and reveals the presence of several photobiont-mediated lichen guilds. Over half of all mycobionts share photobionts with other fungal species, often from different genera or even families, while some others are strict specialists and exclusively associate with a single photobiont variant. The most extensive symbiont network involves 24 different fungal species from five genera associating with 38 Nostoc photobionts. The Nostoc photobionts belong to two main groups, the Nephroma-type Nostoc and the Collema/Peltigera-type Nostoc, and nearly all mycobionts associate only with variants of one group. Among the mycobionts, species that produce cephalodia and those without symbiotic propagules tend to be most promiscuous in photobiont choice. The extent of photobiont sharing and the structure of interaction networks differ dramatically between the two major photobiont-mediated guilds, being both more prevalent and nested among Nephroma guild fungi and more compartmentalized among Peltigera guild fungi. This presumably reflects differences in the ecological characteristics and/or requirements of the two main groups of photobionts. The same two groups of Nostoc have previously been identified from many lichens in various lichen-rich ecosystems in different parts of the world, indicating that photobiont sharing between fungal species is an integral part of lichen ecology globally. In many cases, symbiotically dispersing lichens can facilitate the dispersal of sexually reproducing species, promoting establishment and adaptation into new and marginal habitats and thus driving evolutionary diversification.

Highlights

Lichens are highly successful self-sustaining ecosystems involving lichen-forming fungi and phototrophic algae and/or cyanobacteria (Hawksworth and Grube, 2020)
The estimated coverage of Nephroma guild mycobionts was 96% and that of corresponding cyanobionts 73%, both values being higher than those estimated for the Peltigera guild, i.e., 82 and 47%, respectively
Blast searches with the obtained tRNALeu (UAA) intron (trnL) sequences revealed that three of the Nephroma-type Nostoc variants had been previously amplified from lichen-associated cyanobacteria: Nostoc variant N3 associating with several Sticta species in the Taita Hills has previously been sequenced from a Crocodia in Brazil and several Nephroma species in Japan (Stenroos et al, 2006; Fedrowitz et al, 2012, 2014); variant N7, in Taita Hills associating with Crocodia, Sticta, and Leptogium species, has previously been found from Pseudocyphellaria from Australia, Chile, and New Zealand (Summerfield et al, 2002; Summerfield and Eaton-Rye, 2006); and N18 found in Taita Hills from Sticta sp. 3 is previously reported from several Nephroma species from Japan

Summary

Introduction

Lichens are highly successful self-sustaining ecosystems involving lichen-forming fungi and phototrophic algae and/or cyanobacteria (Hawksworth and Grube, 2020). In the socalled bipartite lichens (Figures 1A,E), the main symbiotic association involves one primary fungus (mycobiont) and photosynthetic algae or cyanobacteria (photobionts). Within Lecanoromycetes (Ascomycota), the largest class of lichen-symbiotic fungi, most mycobionts seem to be highly specific in their choice of photobionts (Dahlkild et al, 2001; Otálora et al, 2010; Dal Grande et al, 2014; Nyati et al, 2014; Leavitt et al, 2015; Chagnon et al, 2018; Jüriado et al, 2019; Dal Forno et al, 2020; Lindgren et al, 2020). The symbiotic partners can either disperse together within symbiotic propagules (Figure 1B) (vertical transmission), or the symbionts reproduce separately; for example, the mycobionts may produce ascospores in apothecia (Figure 1F) and re-establish the symbiotic association after dispersal (horizontal transmission). Many lichens, including some species in most genera of cyanolichens (lichens with cyanobacterial photobionts), utilize both means of dispersal and photobiont transmission

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Conclusion