Nitrogen-Fixing Bacteria Associated with Peltigera Cyanolichens and Cladonia Chlorolichens

Abstract

Lichens have been extensively studied and described; however, recent evidence suggests that members of the bacterial community associated with them could contribute new functions to the symbiotic interaction. In this work, we compare the nitrogen-fixing guild associated with bipartite terricolous lichens with different types of photobiont: Peltigera cyanolichens and Cladonia chlorolichens. Since cyanobacteria contribute nitrogen to the symbiosis, we propose that chlorolichens have more diverse bacteria with the ability to fix nitrogen compared to cyanolichens. In addition, since part of these bacteria could be recruited from the substrate where lichens grow, we propose that thalli and substrates share some bacteria in common. The structure of the nitrogen-fixing guild in the lichen and substrate bacterial communities of both lichens was determined by terminal restriction fragment length polymorphism (TRFLP) of the nifH gene. Multivariate analyses showed that the nitrogen-fixing bacteria associated with both types of lichen were distinguishable from those present in their substrates. Likewise, the structure of the nitrogen-fixing bacteria present in the cyanolichens was different from that of chlorolichens. Finally, the diversity of this bacterial guild calculated using the Shannon index confirms the hypothesis that chlorolichens have a higher diversity of nitrogen-fixing bacteria than cyanolichens.

The Lichens’ Microbiota, Still a Mystery?

“…In the case of N-limiting conditions, bacterial N-fixation, by e.g., Azotobacter , Betaproteobacteria or Alphaproteobacteria, could be of considerable importance for the vitality of lichens ( Leveau and Preston, 2008 ; Grube and Berg, 2009 ; Grube et al, 2009 ; Bates et al, 2011 ; Erlacher et al, 2015 ). This fits well with studies of Almendras et al (2018) showing that Chlorolichens have a higher diversity of N-fixing bacteria than cyanolichens. However, nitrogen supply is not a problem in many parts of Europe, as the atmosphere carries massive amounts of nitrogen compounds from agriculture over large distances.…”

“…Creating a partial anaerobic biofilm as bacterial habitat is important for bacterial nitrogen fixation, which may augment the nitrogen budget in lichens lacking a N-compound-donating cyanobiont. Several lichen-associated bacteria, like Alphaproteobacteria ( Grube et al, 2009 ; Almendras et al, 2018 ), Gammaproteobacteria ( Liba et al, 2006 ), Firmicutes ( Grube et al, 2009 ; Almendras et al, 2018 ) and Actinobacteria ( Almendras et al, 2018 ) contain nifH genes. In the case of N-limiting conditions, bacterial N-fixation, by e.g., Azotobacter , Betaproteobacteria or Alphaproteobacteria, could be of considerable importance for the vitality of lichens ( Leveau and Preston, 2008 ; Grube and Berg, 2009 ; Grube et al, 2009 ; Bates et al, 2011 ; Erlacher et al, 2015 ).…”

Testing carbon and nitrogen sources for the in vitro growth of the model lichenized fungus Endocarpon pusillum Hedw.

“…Lichens form when specific species of fungi contact a compatible photobiont, either a cyanobacterium or eukaryotic green alga (Green & Smith 1974; Almendras et al . 2018). The fungus encapsulates the algal cells and an unidentified inter-kingdom communication alters the algal cell morphology (Joneson & Lutzoni 2009).…”

Unraveling the sugar code: the role of microbial extracellular glycans in plant–microbe interactions

“…Bacterial and basidiomycetous yeast-derived EPSs in lichens are less studied but their potential functions should not be underestimated. Indeed the presence of the nifH gene involved in nitrogen fixation was demonstrated in several lichen-associated α-proteobacteria, γ-proteobacteria, actinobacteria, and firmicutes ( Grube et al ., 2009 ; Almendras et al ., 2018 ). Prominent among the α-proteobacteria are the Rhizobiales with LAR1, a lichen-associated bacterial clade ( Hodkinson and Lutzoni, 2009 ).…”