Christophe Calvaruso

Mineral weathering by bacteria: ecology, actors and mechanisms

Soil microbes play an essential role in the environment by contributing to the release of key nutrients from primary minerals that are required not only for their own nutrition but also for that of plants. Although the role of fungi in mineral weathering is beginning to be elucidated, the relative impact of bacteria in this process and the molecular mechanisms involved remain poorly understood. Here, we discuss the ecological relevance of bacterial weathering, mainly in the soil and especially in acidic forest ecosystems, which strongly depend on mineral weathering for their sustainability. We also present highlights from recent studies showing molecular mechanisms and genetic determinants involved in the dissolution of complex minerals under aerobic conditions. Finally, we consider the potential applications of genomic resources to the study of bacterial weathering.

Effect of the mycorrhizosphere on the genotypic and metabolic diversity of the bacterial communities involved in mineral weathering in a forest soil.

ABSTRACT To date, several bacterial species have been described as mineral-weathering agents which improve plant nutrition and growth. However, the possible relationships between mineral-weathering potential, taxonomic identity, and metabolic ability have not been investigated thus far. In this study, we characterized a collection of 61 bacterial strains isolated from Scleroderma citrinum mycorrhizae, the mycorrhizosphere, and the adjacent bulk soil in an oak forest. The ability of bacteria to weather biotite was assessed with a new microplate bioassay that measures the pH and the quantity of iron released from this mineral. We showed that weathering bacteria occurred more frequently in the vicinity of S. citrinum than in the bulk soil. Moreover, the weathering efficacy of the mycorrhizosphere bacterial isolates was significantly greater than that of the bulk soil isolates. All the bacterial isolates were identified by partial 16S rRNA gene sequence analysis as members of the genera Burkholderia, Collimonas, Pseudomonas, and Sphingomonas, and their carbon metabolism was characterized by the BIOLOG method. The most efficient isolates belonged to the genera Burkholderia and Collimonas. Multivariate analysis resulted in identification of three metabolic groups, one of which contained mainly bacterial isolates associated with S. citrinum and exhibiting high mineral-weathering potential. Therefore, our results support the hypothesis that by its carbon metabolism this fungus selects in the bulk soil reservoir a bacterial community with high weathering potential, and they also address the question of functional complementation between mycorrhizal fungi and bacteria in the ectomycorrhizal complex for the promotion of tree nutrition.

Root-Associated Bacteria Contribute to Mineral Weathering and to Mineral Nutrition in Trees: a Budgeting Analysis

ABSTRACT The principal nutrient source for forest trees derives from the weathering of soil minerals which results from water circulation and from plant and microbial activity. The main objectives of this work were to quantify the respective effects of plant- and root-associated bacteria on mineral weathering and their consequences on tree seedling growth and nutrition. That is why we carried out two column experiments with a quartz-biotite substrate. The columns were planted with or without pine seedlings and inoculated or not with three ectomycorrhizosphere bacterial strains to quantify biotite weathering and pine growth and to determine how bacteria improve pine growth. We showed that the pine roots significantly increased biotite weathering by a factor of 1.3 for magnesium and 1.7 for potassium. We also demonstrated that the inoculation of Burkholderia glathei PML1(12) significantly increased biotite weathering by a factor of 1.4 for magnesium and 1.5 for potassium in comparison with the pine alone. In addition, we observed a significant positive effect of B. glathei PMB1(7) and PML1(12) on pine growth and on root morphology (number of lateral roots and root hairs). We demonstrated that PML1(12) improved pine growth when the seedlings were supplied with a nutrient solution which did not contain the nutrients present in the biotite. No improvement of pine growth was observed when the seedlings were supplied with all the nutrients necessary for pine growth. We therefore propose that the growth-promoting effect of B. glathei PML1(12) mainly resulted from the improved plant nutrition via increased mineral weathering.

Influence of Forest Trees on the Distribution of Mineral Weathering-Associated Bacterial Communities of the Scleroderma citrinum Mycorrhizosphere

ABSTRACT In acidic forest soils, availability of inorganic nutrients is a tree-growth-limiting factor. A hypothesis to explain sustainable forest development proposes that tree roots select soil microbes involved in central biogeochemical processes, such as mineral weathering, that may contribute to nutrient mobilization and tree nutrition. Here we showed, by combining soil analyses with cultivation-dependent analyses of the culturable bacterial communities associated with the widespread mycorrhizal fungus Scleroderma citrinum, a significant enrichment of bacterial isolates with efficient mineral weathering potentials around the oak and beech mycorrhizal roots compared to bulk soil. Such a difference did not exist in the rhizosphere of Norway spruce. The mineral weathering ability of the bacterial isolates was assessed using a microplaque assay that measures the pH and the amount of iron released from biotite. Using this microplate assay, we demonstrated that the bacterial isolates harboring the most efficient mineral weathering potential belonged to the Burkholderia genus. Notably, previous work revealed that oak and beech harbored very similar pHs in the 5- to 10-cm horizon in both rhizosphere and bulk soil environments. In the spruce rhizosphere, in contrast, the pH was significantly lower than that in bulk soil. Because the production of protons is one of the main mechanisms responsible for mineral weathering, our results suggest that certain tree species have developed indirect strategies for mineral weathering in nutrient-poor soils, which lie in the selection of bacterial communities with efficient mineral weathering potentials.

Atmospheric particulate deposition in temperate deciduous forest ecosystems: Interactions with the canopy and nutrient inputs in two beech stands of Northeastern France

As wood harvests are expected to increase to satisfy the need for bio-energy in Europe, quantifying atmospheric nutrient inputs in forest ecosystems is essential for forest management. Current atmospheric measurements only take into account the <0.45 μm fraction and dry deposition is generally modeled. The aims of this study were to quantify atmospheric particulate deposition (APD), the >0.45 μm fraction of atmospheric deposition, below the canopy, to study the influence of the canopy on APD, and to determine the influence of APD below canopy to nutrient input-output budgets with a focus on base cations calcium, magnesium and potassium, and phosphorus. APD was sampled every four weeks by passive collectors. We divided APD into an organic and a mineral fraction, respectively POM and MDD. MDD was divided into a soluble and a hardly soluble fraction in hydrogen peroxide, referred to as S-MDD and H-MDD, respectively. In order to better understand the influence of the canopy on APD, we studied APD in three pathways below the canopy (litterfall, stemflow and throughfall), and in open field. Our results indicated that APD in throughfall (123 ± 64 kg ha(-1)year(-1)) was significantly higher and synchronic with that in open field (33 ±9 kg ha(-1)year(-1)) in the two study sites. This concerned both POM and MDD, suggesting a large interception of APD by foliar surfaces, which is rapidly washed off by rain within four weeks. Throughfall H-MDD was the main pathway with an average of 16 ± 2 kg ha(-1)year(-1). Stemflow and litterfall were neglected. In one study site, canopy intercepted about 8 kg ha(-1)year(-1) of S-MDD. Although base cations and phosphorus inputs by APD are lower than those of <0.45 μm deposition, they contributed from 5 to 32% to atmospheric deposition and improved the nutrient budget in one of the study sites.

Chrysotile dissolution in the rhizosphere of the nickel hyperaccumulator Leptoplax emarginata.

Ni phytoextraction processes need further understanding of the interactions between Ni availability in soils and its absorption by plant roots. The large metal uptake and root exudation by hyperaccumulator species could accelerate the weathering process of Ni-bearing phases in the rhizosphere. The aim of this work was to quantify the weathering of a Ni-bearing mineral phase in the rhizosphere of the Ni-hyperaccumulator Leptoplax emarginata. The studied mineral was chrysotile which was characterized by a low Ni solubility. Column experiments were performed to assess the effect of the Ni-hyperaccumulator L. emarginata and the contribution of rhizobacteria on the dissolution rate of chrysotile. Mineral weathering was monitored by measuring Ni and Mg transferred to leachates or plants throughout the experiment. Results showed that L. emarginata increased chrysotile dissolution by more than 2-fold . The hyperaccumulator L. emarginata accumulated 88% on average of total mobilized Ni. Inoculation with Ni-resistant bacteria in the rhizosphere of L. emarginata had no significant effect on chrysotile dissolution or plant accumulation of Ni in this context. Finally, after 15 weeks of culture, 1.65% of total Ni in the system was mobilized in the planted treatments compared with 0.03% in the unplanted treatments.