Complex photobiont diversity in the marine lichen Lichina pygmaea

Nathan A M Chrismas,Anita L Hollingsworth,Michael Cunliffe,Ro Allen,Joe D Taylor

doi:10.1017/s002531542100062x

Abstract

AbstractLichens are a well-known symbiosis between a host mycobiont and eukaryote algal or cyanobacterial photobiont partner(s). Recent studies have indicated that terrestrial lichens can also contain other cryptic photobionts that increase the lichens’ ecological fitness in response to varying environmental conditions. Marine lichens live in distinct ecosystems compared with their terrestrial counterparts because of regular submersion in seawater and are much less studied. We performed bacteria 16S and eukaryote 18S rRNA gene metabarcoding surveys to assess total photobiont diversity within the marine lichen Lichina pygmaea (Lightf.) C. Agardh, which is widespread throughout the intertidal zone of Atlantic coastlines. We found that in addition to the established cyanobacterial photobiont Rivularia, L. pygmaea is also apparently host to a range of other marine and freshwater cyanobacteria, as well as marine eukaryote algae in the family Ulvophyceae (Chlorophyta). We propose that symbiosis with multiple freshwater and marine cyanobacteria and eukaryote photobionts may contribute to the ability of L. pygmaea to survive the harsh fluctuating environmental conditions of the intertidal zone.

Highlights

Lichen symbiosis is undergoing renewed scrutiny, in part because of the application of molecular ecology techniques such as metabarcoding (Hawksworth & Grube, 2020; Smith et al, 2020)
Cyanobacteria dominated the bacterial community within all three thalli accounting for up to 49% of 16S rRNA gene reads (Figure 2A), while the green algae family Ulvophyceae (Chlorophyta) dominated the intrathalline eukaryotic community, accounting for up to 82% of the 18S rRNA gene reads (Figure 2A)
Enriched amplicon sequence variants (ASVs), ASV_6 (MZ169869), ASV_18 (MZ169873) and ASV_55 (MZ169883) accounting for up to 8.7, 4.6 and 1.5% of the intrathalline bacterial community respectively, and a fourth ASV_73 (MZ169887), which was only found at Rame Head where it comprised up to 6.1% of the community, all belonged to Rivularia, the established L. pygmaea photobiont (Ortiz-Álvarez et al, 2015)

Summary

Introduction

Lichen symbiosis is undergoing renewed scrutiny, in part because of the application of molecular ecology techniques such as metabarcoding (Hawksworth & Grube, 2020; Smith et al, 2020). Historic assumptions about the ‘single fungus and single eukaryote alga or Cyanobacteria’ nature of the symbiosis do not take into account tripartite lichens (i.e., those containing cyanobacterial and algal photobionts) (Rikkinen et al, 2002; Henskens et al, 2012), and have been further challenged by the more recent discovery of other fungi (Millanes et al, 2016; Spribille et al, 2016; Mark et al, 2020), eukaryote algae (chlorobionts) and Cyanobacteria (cyanobionts) (Henskens et al, 2012; Moya et al, 2017) within lichens in addition to the primary myco- and photobionts (Smith et al, 2020), alongside a complex diversity of heterotrophic bacteria (Grube et al, 2009) This increased diversity of organisms co-existing within the lichen thallus has added support to an ongoing reinterpretation of lichens as even more complex ecological associations comprising numerous interacting components (Honegger, 1991; Hawksworth & Grube, 2020). Photobiont ‘switching’ may allow for a further increase in fitness where multiple mycobiont lineages share locally adapted photobiont genotypes (Piercey-Normore & DePriest, 2001)

Methods

Results

Conclusion