&lt;i&gt;In-planta&lt;/i&gt; Sporulation Capacity Enhances Infectivity and Rhizospheric Competitiveness of &lt;i&gt;Frankia&lt;/i&gt; Strains

Pozzi

Gareil

et al. 2017

PeerJ

Self Cite

BackgroundRecent climatic history has strongly impacted plant populations, but little is known about its effect on microbes. Alders, which host few and specific symbionts, have high genetic diversity in glacial refugia. Here, we tested the prediction that communities of root symbionts survived in refugia with their host populations. We expected to detect endemic symbionts and a higher species richness in refugia as compared to recolonized areas.MethodsWe sampled ectomycorrhizal (EM) root tips and the nitrogen-fixing actinomycete Frankia communities in eight sites colonized by Alnus glutinosa subsp. barbata close to the Caucasus in Georgia. Three sites were located in the Colchis, one major Eurasian climatic refugia for Arcto-Tertiary flora and alders, and five sites were located in the recolonized zone. Endemic symbionts and plant ITS variants were detected by comparing sequences to published data from Europe and another Tertiary refugium, the Hyrcanian forest. Species richness and community structure were compared between sites from refugia and recolonized areas for each symbionts.ResultsFor both symbionts, most MOTUs present in Georgia had been found previously elsewhere in Europe. Three endemic Frankia strains were detected in the Colchis vs two in the recolonized zone, and the five endemic EM fungi were detected only in the recolonized zone. Frankia species richness was higher in the Colchis while the contrary was observed for EM fungi. Moreover, the genetic diversity of one alder specialist Alnicola xanthophylla was particularly high in the recolonized zone. The EM communities occurring in the Colchis and the Hyrcanian forests shared closely related endemic species.DiscussionThe Colchis did not have the highest alpha diversity and more endemic species, suggesting that our hypothesis based on alder biogeography may not apply to alder’s symbionts. Our study in the Caucasus brings new clues to understand symbioses biogeography and their survival in Tertiary and ice-age refugia, and reveals that isolated host populations could be of interest for symbiont diversity conservation.

Section: Introductionmentioning

confidence: 99%

Alder and the Golden Fleece: high diversity of Frankia and ectomycorrhizal fungi revealed from Alnus glutinosa subsp. barbata roots close to a Tertiary and glacial refugium

Pozzi

Gareil

et al. 2017

PeerJ

Self Cite

“…The production of abundant asexual spores, which have high potential for propagation and for resistance to unfavorable conditions, may play an important role in the microbe's fitness and biogeography. Thus, the huge number of spores produced by Spϩ Frankia strains may enhance both their survival and dispersion capacity and could therefore explain their high infectivity and competitiveness on host plant roots compared to SpϪ strains (15). In addition, spore production may compete with nitrogen fixation by using part of the plant's investment (photosynthesis products and energy) in the nodules and by occupying the infected cells with spores instead of diazovesicles (the specialized cells where nitrogen fixation occurs), thus limiting the benefits for the plant (14).…”

mentioning

confidence: 99%

In Planta Sporulation of Frankia spp. as a Determinant of Alder-Symbiont Interactions

Schwob

Pozzi

et al. 2018

Appl Environ Microbiol

The genus forms symbiosis with the actinobacteria spp. and ectomycorrhizal fungi. Two types of lineages can be distinguished based on their ability to sporulate Spore-positive (Sp+) strains are predominant on and in highlands, while spore-negative (Sp-) strains are mainly associated with in lowlands. Here, we investigated whether the Sp+ predominance in nodules is due to host selection of certain genotypes from soil communities or the result of the ecological history of the alder stand soil, as well as the effect of the sporulation genotype on the ectomycorrhizal (ECM) communities. Trapping experiments were conducted using ,, and plantlets on 6 soils, differing in the alder species and the frequency of Sp+ nodules in the field. Higher diversity of spp. and variation in Sp+ frequencies were observed in the trapping than in the fields. Both indigenous and trapping species shape community structure in trapped nodules. Nodulation impediments were observed under several trapping conditions in Sp+ soils, supporting a narrower host range of Sp+ species. and were able to associate equally with compatible Sp+ and Sp- strains in the greenhouse. Additionally, no host shift was observed for -specific ECM, and the sporulation genotype of spp. defined the ECM communities on the host roots. The symbiotic association is likely determined by the host range, the soil history, and the type of species. These results provide an insight into the biogeographical drivers of alder symbionts in the Holarctic region. Most -actinorhiza plant symbioses are capable of high rates of nitrogen fixation comparable to those found on legumes. Yet, our understanding of the ecology and distribution of spp. is still very limited. Several studies have focused on the distribution patterns of spp., demonstrating a combination of host and pedoclimatic parameters in their biogeography. However, very few have considered the sporulation form of the strain, although it is a unique feature among all symbiotic plant-associated microbes. Compared with Sp- strains, Sp+ strains would be obligate symbionts that are highly dependent on the presence of a compatible host species and with lower efficiency in nitrogen fixation. Understanding the biogeographical drivers of Sp+ strains might help elucidate the ecological role of sporulation and the extent to which this trait mediates host-partner interactions in the alder--ECM fungal symbiosis.

“…These studies suggest that there is variable host dependency of symbiotic Frankia strains. Moreover, the capacity of Frankiae to disperse and survive in soils could depend on its capacity to sporulate (Cotin‐Galvan et al ., ). Two phenotypes of Frankia strains are distinguished based on the ability to form abundant spores in root‐nodule cells: spore‐positive (Sp+) which are likely obligate symbionts and spore‐negative (Sp–) more adapted to saprophytic life.…”

Section: Introductionmentioning

confidence: 97%

“…Several studies have suggested that aboveground-belowground relationships are stronger for fungi compared to bacteria because the latter are supposed less dependent for survival on the plant hosts (Gao et al, 2013;Prober et al, 2015). However, the case of symbiotic bacteria highly dependent on their host such as Sp1 Frankia strains has not been investigated Cotin-Galvan et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Green alder (Alnus viridis) encroachment shapes microbial communities in subalpine soils and impacts its bacterial or fungal symbionts differently

Schwob

Environmental Microbiology

Manzi

et al. 2017

Since the mid-twentieth century, subalpine grasslands undergo a progressive encroachment by Alnus viridis shrubs. Thanks to its rapid vegetative reproduction, its nitrogen fixing symbiosis with Frankia and its ectomycorrhizal cohorts, green alders are vigorous colonizers that quickly form mosaic of alder patches that evolves into a close canopy shrub community. To better understand how alder encroachment might influence microbial communities in this successional sequence, symbiont distribution, microbial richness and community structure in both soils and nodules were analyzed at three successional stages: grassland, mosaic and forest. Soil analyses were performed in association with measures of nitrification and denitrification, as well as DNA metabarcoding of three bacterial genes (16S rDNA, nifH and amoA) and one fungal gene (ITS1). Our results show that (i) A. viridis encroachment is associated with soil microbial community changes that are in turn, linked to certain soil properties (i.e., pH, C/N ratio and organic matter content), (ii) both taxonomic and N related functional gene structures of bacteria are modified by alder encroachment and (iii) the distribution in soils of its bacterial symbionts (Frankia) is apparently weakly influenced by alder establishment while Alnus-specific ectomyccorrhizae increase with the increase in alder shrub density.