Feathermoss and epiphytic Nostoc cooperate differently: expanding the spectrum of plant–cyanobacteria symbiosis

Abstract

Dinitrogen (N2)-fixation by cyanobacteria in symbiosis with feathermosses is the primary pathway of biological nitrogen (N) input into boreal forests. Despite its significance, little is known about the cyanobacterial gene repertoire and regulatory rewiring needed for the establishment and maintenance of the symbiosis. To determine gene acquisitions and regulatory changes allowing cyanobacteria to form and maintain this symbiosis, we compared genomically closely related symbiotic-competent and -incompetent Nostoc strains using a proteogenomics approach and an experimental set up allowing for controlled chemical and physical contact between partners. Thirty-two gene families were found only in the genomes of symbiotic strains, including some never before associated with cyanobacterial symbiosis. We identified conserved orthologs that were differentially expressed in symbiotic strains, including protein families involved in chemotaxis and motility, NO regulation, sulfate/phosphate transport, and glycosyl-modifying and oxidative stress-mediating exoenzymes. The physical moss–cyanobacteria epiphytic symbiosis is distinct from other cyanobacteria–plant symbioses, with Nostoc retaining motility, and lacking modulation of N2-fixation, photosynthesis, GS-GOGAT cycle and heterocyst formation. The results expand our knowledge base of plant–cyanobacterial symbioses, provide a model of information and material exchange in this ecologically significant symbiosis, and suggest new currencies, namely nitric oxide and aliphatic sulfonates, may be involved in establishing and maintaining the cyanobacteria–feathermoss symbiosis.

Novel bacterial lineages associated with boreal moss species

“…However, it is also possible that WPS‐2 could be capable of sulfide‐based anoxygenic phototrophy by obtaining sulfur from organic compounds provided by the moss, as was proposed by Warshan et al . () for interactions between feather mosses and their Cyanobacteria . If WPS‐2 is an AAP or a FAP, it would be one of the few observed lineages to possess RuBisCo.…”

“…Neither FAPs nor AAPs depend on sulfur for growth and both have the potential to survive in aerobic or microaerobic conditions, though FAPs cannot grow photoautotrophically in fully aerobic conditions (Madigan et al, 2017;Yurkov and Hughes, 2017). However, it is also possible that WPS-2 could be capable of sulfide-based anoxygenic phototrophy by obtaining sulfur from organic compounds provided by the moss, as was proposed by Warshan et al (2017) for interactions between feather mosses and their Cyanobacteria. If WPS-2 is an AAP or a FAP, it would be one of the few observed lineages to possess RuBisCo.…”

A plant perspective on nitrogen cycling in the rhizosphere

“…These symbiotic cyanobacteria can enter epiphytic and intracellular or extracellular endophytic interactions with their host. In boreal forests, this N 2 fixation by cyanobacteria living in symbiosis with mosses can account to up to 50% of total biological N input (DeLuca, Zackrisson, Nilsson, & Sellstedt, ; Santi et al, ; Warshan et al, ). In N‐depleted soils in Mexico, recent work has shown that the mucilage of aerial roots of an indigenous landrace of maize enriched in diazotrophs (Van Deynze et al, ) (Figure ).…”

“…These symbiotic cyanobacteria can enter epiphytic and intracellular or extracellular endophytic interactions with their host. In boreal forests, this N 2 fixation by cyanobacteria living in symbiosis with mosses can account to up to 50% of total biological N input (DeLuca, Zackrisson, Nilsson, & Sellstedt, 2002;Santi et al, 2013;Warshan et al, 2017).…”

Differential gene expression associated with fungal trophic shifts along the senescence gradient of the moss Dicranum scoparium

“…4). Although the mechanisms for N transfer from these N-fixing bacteria to mosses (Warshan et al, 2017) remain to be fully characterized, fungi might take advantage of the mossbacteria association to obtain nitrogen. Fungi-bacteria-moss interactions appear to be complex and might involve other organisms, such as arthropod and algae that also inhabit mosses (Andrew et al, 2003;Knapp and Lowe, 2009;Feng et al, 2016).…”