Genomic Era Tools Pry Secrets from Plants and their Intimate Microbial Companions

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Populus flower – Image Source: Virginia Tech, Forest Resources and Environmental Conservation

Yet another plant has been caught actively recruiting its microbial companions, this time it’s an eastern cottonwood tree more formally known as Populus deltoides.

Using new high-throughput pyrosequencing of bacterial and fungal rRNA gene markers, Christopher W. Schadt at the Oak Ridge National Laboratory in Tennessee and colleagues there as well as Duke University in Durham, North Carolina report that the microbial communities in Populus are distinct assemblages and not passively acquired opportunists from the surrounding soil. This work, like research on sugar beets and legumes, challenges the long-held belief that soil properties determine the distribution and composition of microbial communities.

“Previous studies have looked at fungi, bacteria, the rhizosphere and the endosphere separately; but pyrosequencing has allowed us to look at all of these together, and this is a first,” Schadt explains.

Studying Populus in its natural setting

Populus Tree – Image Source: Virginia Tech, Dept. of Forest Resources and Environmental Conservation

Populus, a favorite of plant scientists, is unusual in that it hosts both arbuscular mycorrhizal fungi (AMF) and ectomycorrhizal fungi (EMF) as well as a number of other endophytic and rhizospheric microbes. However, says Schadt, “Very little is known about Populus interactions with microbial communities in nature as most studies have focused on greenhouse cuttings or short-rotation, plantation grown trees.”  Importantly, this is one of the very few investigations using culture-independent methods; notably, the majority of the world’s microbes will not grow in captivity thus culturing is notoriously inaccurate.

“While more soils and sites need to be tested, the tree-associated consortia of fungi and bacteria we investigated were remarkably and unexpectedly consistent across two completely different locations and soils, one upland and another bottomland,” Schadt says.

Endophytic microbes are not a subset of the rhizosphere community

Rhizopheric and endophytic microbial communities colonizing wild Populus were clearly different, suggesting that the tissues inside Populus roots represent a unique niche for microbes,” Schadt says. While EMF was more abundant than AMF both in and around Populus roots, there were greater numbers of EMF from the Agaricomcotina in their rhizospheres than their endospheres. Additionally, the most frequently found endophytic bacteria in Populus were Gammaproteobacteria and Alphaproteobacteria whereas Acidobacteria was more common than Gammaproteobacteria in the rhizosphere.

Even more telling, says Neil R. Gottel, Schadt’s colleague at Oak Ridge and the study’s lead investigator, “A single Pseudomonas-like species accounted for 34% of the endophytic bacterial sequences, but was extremely rare just millimeters away in the rhizosphere soil.”

AMF host their own endosymbionts –and they’re bacterial

Populus isn’t the only tree to partner with AMF, or Glomeromycota, which are “obligate endophytic symbionts of most trees as well as wild grasses and food crops on earth,” says the University of Turin’s Paola Bonfante.  Bonfante and her colleagues in Italy recently discovered that the AMF, Gigaspora margarita has its own endosymbionts and they’re bacterial. Some are round (coccoid) and related to Mollicutes others are rods called Candidatus Glomeribacter gigasporarum (CaGg) which are kin to Burkholderia.

CaGg extremely dependent on its host for food and energy and in return makes the fungus more fit

Using Sanger sequencing and shotgun 454 pyrosequencing, these researchers explored the CaGg genome and report that “it’s strikingly reduced when compared to its free-living relatives and similar to many insect endosymbionts, including those able to manipulate host reproductive functions.”

Its skimpy genome renders CaGg dependent on the fungal host for both energy and nutrition and in return the bacteria synthesize vitamin B10 as well as antibiotic- and toxin- resistance molecules which helps make the fungus more fit. “This is an entirely novel and intimate symbiosis,” says Bonfante emphasizing that the fungal host is itself an “obligate biotrop” that relies on its photosynthetic plant for food and shelter.  “Our work represents the first step towards uncovering the complex network of intimate interactions between plants, AMF and endobacteria,” she adds.

Plants, AMF and endobacteria -ancient and enduring relationships

Mycelia of an AMF emerging from a plant root – Image Source: E.V. Johnson, University of Hawaii at Mãnoa

The association between AMF and plants is ancient, dating back to the colonization of land by terrestrial plants at least 400 million years ago. In fact, it is widely accepted that ancestral AMF assisted plants in their “greening of the earth,” an idea that has been recently confirmed by David J. Beerling at the University of Sheffield in the UK and colleagues at the University of Sydney in Australia, the Imperial College London and the Royal Botanic Gardens, Kew, in the UK. Their work with the most ancient extant clade of land plants, the complex thalloid liverwort, showed that the mutualistic symbiosis by AMFs improved plant growth and fitness.  Liverworts in symbiotic relationships with AMFs were more fit than those that weren’t showing enhanced photosynthesis and better growth.

Moreover, it appears that at least one of AMF’s bacterial endosymbionts –a  little round bacterium related to the Mollicutes—has been witness to and probably helpers in the greening of the earth.  According to Bonfante and collaborators, “These bacteria split from their sister groups more than 400 million years ago, colonizing their fungal hosts before the main AMF lineages separated.” The bacterial-AMF symbiosis can, therefore, “be dated back to at least the time when AMF formed the ancestral symbiosis with emergent land plants,” she adds.

 Personal communications:  Christopher W. Schadt, PhD and Paola Bonfante, PhD.

 Additional sources:

Bonfante P. and Requena N. Dating in the dark: how roots respond to fungal signals to establish arbuscular mycorrhizal symbiosis. (2011); Current Opinion in Plant Biology: 14, 1-7.

Bonfante P. and Genre A.  Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. (2010); Nature Communications: 1:48/DOI: 10.1038/ncomms1046.

Ghignone S., Salvioli A., Anca I., et alThe genome of the obligate endobacterium of an AM fungus reveals an interphylum network of nutritional interactions. (2011); ISME J.doi: 10.1038/ismej.2011.110.

Gottel N.R., Castro H.F., Kerley M., et al. Distinct Microbial Communities within the Endosphere and Rhizosphere of Populus deltoides Roots across Contrasting Soil Types. (2011); Applied and Environmental Microbiology: 77 (17) 5934-5944.

Humphreys C.P., Franks P.J., Rees M., et al. Mutualistic mycorrhiza-like symbiosis in the most ancient group of land plants. (2010). Nature Communications: 1:103/DOI:10.1038/ncomms1105.

Naumann M., Schüssler A., Bonfante P. The obligate endobacteria of arbuscular mycorrhizal fungi are ancient heritable components related to the Mollicutes. (2010) ISME J: 4 (7):862-871

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