Bacterial Communities Associated with Flowering Plants of the Ni Hyperaccumulator Thlaspi goesingense

Abstract

Thlaspi goesingense is able to hyperaccumulate extremely high concentrations of Ni when grown in ultramafic soils. Recently it has been shown that rhizosphere bacteria may increase the heavy metal concentrations in hyperaccumulator plants significantly, whereas the role of endophytes has not been investigated yet. In this study the rhizosphere and shoot-associated (endophytic) bacteria colonizing T. goesingense were characterized in detail by using both cultivation and cultivation-independent techniques. Bacteria were identified by 16S rRNA sequence analysis, and isolates were further characterized regarding characteristics that may be relevant for a beneficial plant-microbe interaction-Ni tolerance, 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase and siderophore production. In the rhizosphere a high percentage of bacteria belonging to the Holophaga/ Acidobacterium division and ␣-Proteobacteria were found. In addition, high-G؉C gram-positive bacteria, Verrucomicrobia, and microbes of the Cytophaga/Flexibacter/Bacteroides division colonized the rhizosphere. The community structure of shoot-associated bacteria was highly different. The majority of clones affiliated with the Proteobacteria, but also bacteria belonging to the Cytophaga/Flexibacter/Bacteroides division, the Holophaga/ Acidobacterium division, and the low-G؉C gram-positive bacteria, were frequently found. A high number of highly related Sphingomonas 16S rRNA gene sequences were detected, which were also obtained by the cultivation of endophytes. Rhizosphere isolates belonged mainly to the genera Methylobacterium, Rhodococcus, and Okibacterium, whereas the majority of endophytes showed high levels of similarity to Methylobacterium mesophilicum. Additionally, Sphingomonas spp. were abundant. Isolates were resistant to Ni concentrations between 5 and 12 mM; however, endophytes generally tolerated higher Ni levels than rhizosphere bacteria. Almost all bacteria were able to produce siderophores. Various strains, particularly endophytes, were able to grow on ACC as the sole nitrogen source.Plants have acquired different mechanisms for growth in the presence of heavy metal concentrations usually considered phytotoxic. One strategy includes the accumulation of extremely large amounts of heavy metals. Hyperaccumulating plants are particularly interesting for phytoremediation technologies for the treatment of metal-polluted soils, sediments, and water resources (40). Several hundred plant species endemic to metalliferous soils have been identified as hyperaccumulators, of which 75% are able to hyperaccumulate Ni when growing in ultramafic soils (5). Thlaspi goesingense Há-lácsy was first described as a hyperaccumulator by Reeves and Brooks (46), and plants grown in an ultramafic soil contained Ni concentrations as high as 12,400 g g Ϫ1 of shoot dry biomass Ϫ1 (56). Although a number of authors have addressed rhizosphere processes of hyperaccumulators, various questions still remain unanswered. Several studies indicated that rhizosphere acidification is no...

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