The Influence of the Host Plant Is the Major Ecological Determinant of the Presence of Nitrogen-Fixing Root Nodule Symbiont Cluster II Frankia Species in Soil

Abstract

The actinobacterial genus Frankia establishes nitrogen-fixing root nodule symbioses with specific hosts within the nitrogen-fixing plant clade. Of four genetically distinct subgroups of Frankia, cluster I, II, and III strains are capable of forming effective nitrogen-fixing symbiotic associations, while cluster IV strains generally do not. Cluster II Frankia strains have rarely been detected in soil devoid of host plants, unlike cluster I or III strains, suggesting a stronger association with their host. To investigate the degree of host influence, we characterized the cluster II Frankia strain distribution in rhizosphere soil in three locations in northern California. The presence/absence of cluster II Frankia strains at a given site correlated significantly with the presence/absence of host plants on the site, as determined by glutamine synthetase (glnA) gene sequence analysis, and by microbiome analysis (16S rRNA gene) of a subset of host/nonhost rhizosphere soils. However, the distribution of cluster II Frankia strains was not significantly affected by other potential determinants such as host-plant species, geographical location, climate, soil pH, or soil type. Rhizosphere soil microbiome analysis showed that cluster II Frankia strains occupied only a minute fraction of the microbiome even in the host-plant-present site and further revealed no statistically significant difference in the ␣-diversity or in the microbiome composition between the host-plantpresent or -absent sites. Taken together, these data suggest that host plants provide a factor that is specific for cluster II Frankia strains, not a general growthpromoting factor. Further, the factor accumulates or is transported at the site level, i.e., beyond the host rhizosphere.IMPORTANCE Biological nitrogen fixation is a bacterial process that accounts for a major fraction of net new nitrogen input in terrestrial ecosystems. Transfer of fixed nitrogen to plant biomass is especially efficient via root nodule symbioses, which represent evolutionarily and ecologically specialized mutualistic associations. Frankia spp. (Actinobacteria), especially cluster II Frankia spp., have an extremely broad host range, yet comparatively little is known about the soil ecology of these organisms in relation to the host plants and their rhizosphere microbiomes. This study reveals a strong influence of the host plant on soil distribution of cluster II Frankia spp.

Frankia-Enriched Metagenomes from the Earliest Diverging Symbiotic Frankia Cluster: They Come in Teams

“…This phenomenon might instead be ascribed to the low saprotrophic potential of cluster-2 Frankia . While there is evidence that cluster-2 strains can occasionally occur in the soil in the absence of their host plant species, this seems to be rare (Battenberg et al. 2017).…”

“…These findings raise several questions. First, the fact that Dg2 represents a metagenome while Dg1 represents a single Frankia strain provides further evidence that in the field, cluster-2 strains exist as assemblages and that different member strains dominate in nodules of different host plants, as indicated in Frankia strain marker analyses in host and nonhost rhizosphere soils (Battenberg et al. 2017).…”

“…On the other hand, cluster-2 strains might occur in the field as single strains or assemblages. Second, if an assemblage of cluster-2 strains infects a host species, is the identity and contribution of the dominant strains dependent on the assemblage, as suggested by Battenberg et al. (2017), or on the host species?…”

Frankia Diversity in Host Plant Root Nodules Is Independent of Abundance or Relative Diversity of Frankia Populations in Corresponding Rhizosphere Soils

“…Existing native prairie remnants contain C. americanus and the corresponding, detectable soil frankiae specific to cluster 2 (24). It has been speculated that cluster 2 frankiae depend on their host plants for growth and establishment (24,37), and thus, the conversion of native vegetation almost entirely to agricultural and urban uses, primarily the cultivation of maize, legume hay crops, and, in recent decades, soybeans may have resulted in the loss of cluster 2 frankiae at this site and other cultivated sites in this region. qPCR data for soil Frankia populations were not exactly matched by targeted Illumina sequencing, which retrieved sequences representing clusters 1a, 1b, 1e, and 3, with all samples dominated by cluster 3 sequences, a small number of cluster 1e reads, and very similar composition of specific reads (Fig.…”

The soil microbiomics of intact, degraded and partially-restored semi-arid succulent thicket (Albany Subtropical Thicket)

“…The intact biomarker taxa were derived from the families Acidobacteriaceae (Subgroup 1) and Myxococcaceae, the order Frankiales and the class Verrucomicrobiae. The order Frankiales is one of the most abundant in the dataset and includes many root-nodule associated taxa (Pawlowski & Demchenko, 2012;Battenberg et al, 2017); its over-representation in intact sites suggests that the changes in the soil microbiome may be due to the reduction or disappearance of plant-associated taxa with the loss of vegetation. By comparison, biomarker taxa for degraded zone soils were the genera Ensifer and Exiguobacterium, members of which are found in diverse environments (Kasana & Pandey, 2018), the cyanobacterial family Coleofasiculaceae, the order Puniceispiralles and the Chloroflexi class Anaerolineae, commonly found in anaerobic digesters (Xia et al, 2016).…”