Current Project: Impact of Climate Change and Elevated Soil Arsenic on Rice Production

We currently investigate how climate change in combination with elevated soil arsenic contamination affect rice production around the world. Soil and seed from Bangladesh, Cambodia and California are used as representative models for two main rice producing regions in the world. Today's climate in terms of temperature and atmospheric CO2 concentration is contrasted to the worst case climate scenario of the year 2100 suggested by the Intergovernmental Panel on Climate Change (IPCC) in 2013. In terms of soil arsenic, today's background concentration of arsenic in paddy soils is compared to a range of concentrations that could potentially be accumulated in the year 2100 considering the increase of soil arsenic that already happened for the past 30 years. Experiments range from greenhouse studies to laboratory experiments, and from wet geochemical measurements to microbial community investigations and sychrotron mineral analysis.
 
 
Investigating how climate change in combination with elevated soil arsenic affect rice productivity and grain quality.
Rice plants are grown to full maturity in pots in the greenhouse to assess the yield and the quality of the grain when the plants are exposed to climate change and elevated soil arsenic. To better understand what is happening in the rhizospheres of rice plants when exposed to these conditions, rice is also grown in custom made rhizotrons. Soil and pore water geochemical data is correlated with plant physiological data and soil microbial community data to understand which stressor, climate or arsenic, affect which component in this rice-paddy soil-microbial community relationship most. The dataset can be used to identify components in this triangular relationship that need optimization to mitigate losses due to a changing climate or elevated soil arsenic.




Soil microcosms are set up in the laboratory to investigate 1. how climate change affects the mobility of arsenic in the soil, and 2. how greenhouse gas emissions from paddy soils in the future will change due to climate change and elevated soil arsenic. Here, microbial community activity and function analysis plays a crucial role in understanding the observed shifts in arsenic mobility and greenhouse gas emissions. 
   

 
   
Microbial communities involved in the formation of iron plaque around rice roots are enriched from rice plants grown under the different climates. These model organisms can be used to investigate what factors increase iron plaque formation around the roots and how arsenic sequestration by the plaque can be increased. The ultimate goal is to reduce arsenic uptake by rice. 


Microbially-Assisted Phytoremediation

  The Phytoremediator plant Arabidopsis halleri was grown on cadmium-contaminated soil in the presence and absence of the natural microbial soil community (A). The amount of accumulated cadmium in the above-ground green tissue of the plant deceased by half in the absence of an established and well-functioning soil microbial community (B). In order to understand differences in microbial community composition present in set-ups with, root bags where employed to separate the bulk soil microbial community from rhizosphere microbial community (C). Microbial taxa of higher relative sequence abundance were identified in the rhizosphere of A. halleri grown on soil with the native microbial community compared to a perturbed microbial community (D), which allows to hypothesize on their potential effect on plant metal uptake.


  • Muehe, E. M.; Weigold, P.; Adaktylou, I. J.; Planer-Friedrich, B.; Kraemer, U.; Kappler, A.; Behrens, S., Rhizosphere microbial community composition affects cadmium and zinc uptake of the metal-hyperaccumulating plant Arabidopsis halleri. Applied and Environmental Microbiology 2015, 81, (6), 2173-2181.
  • Muehe, E. M.; Kappler, A., Biogene Eisenminerale kontrollieren das Umweltverhalten toxischer Metalle. BIOspektrum 2016, 22, (3), 316-318.

Metal-Contaminant Mobility during Iron Redox Cycling


New insights into the fate of cadmium in reducing environments.
An overall loss of cadmium mobility (A) was linked to the reduction of iron (B) in water-logged soils, which was attributed to an increased presence of the iron reducing taxa Geobacter spp. (C). When co-localizing different elements in soil particles using a SEM-EDX mapping (Scanning electron microscope energy dispersive X-ray spectroscopy),  cadmium was shown to be transferred to minor calcium and sulfur mineral phases as indicated by the red and blue arrows in panel (D). Most of the cadmium though was transferred to an iron mineral phase that did not correlate to any other element, thus, most likely cadmium was co-localized to the iron(II)/(III) oxide magnetite. 

These experiments also led to the isolation of a new Geobacter sp. strain Cd1 (E). This strain was used as a model organism to investigate mobility shifts of cadmium during iron(III)-reduction, as it is able to reduce iron(III) minerals up to the presence of 112 mg cadmium per liter (F). During the initial microbial reduction of cadmium-loaded ferrihydrite, sorbed cadmium is mobilized (G). During continuous microbial iron(III) reduction, cadmium was immobilized (D) by sorption to and/or coprecipitation within newly formed secondary minerals as demonstrated by STXM (Scanning transmission X-ray microscopy) (H). Mössbauer analysis besides other supporting techniques confirmed that cadmium was associated with calcium, iron and carbonates, implying the formation of an otavite-siderite-calcite (CdCO3−FeCO3−CaCO3) mixed mineral phase (I).

Currently we are investigating whether and to what extent cadmium is incorporated into biogenically formed magnetite.



 

  • Muehe, E. M.; Adaktylou, I. J.; Obst, M.; Zeitvogel, F.; Behrens, S.; Planer-Friedrich, B.; Kraemer, U.; Kappler, A., Organic carbon and reducing conditions lead to cadmium immobilization by secondary Fe mineral formation in a pH neutral soil. Environmental Science and Technology 2013, 47, 13430−13439.
  • Muehe, E. M.; Obst, M.; Hitchcock, A. P.; Tylsizczak, T.; Behrens, S.; Schröder, C.; Byrne, J. M.; Michel, M.; Kraemer, U.; Kappler, A., Fate of Cd during microbial Fe(III) mineral reduction by a novel and Cd-tolerant Geobacter species. Environmental Science and Technology 2013, 47, 14099-14109.
  • Muehe, E. M.; Kappler, A., Biogene Eisenminerale kontrollieren das Umweltverhalten toxischer Metalle. BIOspektrum 2016, 22, (3), 316-318.

 


Iron minerals play a big role for the mobility of arsenic in the environment. To date, research has focused on the reactivity of abiogenic iron(III) (oxyhydr)oxides, yet in nature biogenic iron(III) (oxyhydr)oxides are more common. Such minerals are for example formed by iron(II)-oxidizing bacteria, and contain organic carbon and exhibit different reactivities and surface properties compared to their abiogenic counterparts. Our studies showed that the extent of iron(III) reduction by Shewanella oneidensis MR-1 of biogenic iron(III) minerals lay in between the reduction of abiotic goethite and ferrihydrite (A), and that arsenic during this process was more effectively and immediately immobilized (B).  This suggests that it is essential to consider both biogenic and abiogenic iron(III) minerals in laboratory studies to fully understand the fate of arsenic in the environment.
In these experiments, a number of different secondarily forming iron mineral phases were precipitated during and after microbial iron(III) reduction of the initial biogenic and abiotic iron minerals (differently colored arrows in C indicate

different mineral morphologies). Iron EXAFS (Extended X-ray absorption fine structure spectroscopy) analysis showed that iron phosphates, including vivianite, were formed after reduction of biogenic iron(III) minerals (D).  In fact, arsenate partially replaced phosphate in vivianite as displayed in the SEM-EDX image in (E), forming a vivianite-symplesite solid solution identified as Fe3(PO4)1.7(AsO4)0.3·8H2O.
  • Muehe, E. M.; Gerhardt, S.; Schink, B.; Kappler, A., Ecophysiology and the energetic benefit of mixotrophicFe(II) oxidation by various strains of nitrate-reducing bacteria. FEMS Microbiology Ecology 2009, 70, (3), 335-343.
  • Kleinert, S.; Muehe, E. M.; Posth, N. R.; Dippon, U.; Daus, B.; Kappler, A., Biogenic Fe(III) minerals lower the efficiency of iron-mineral-based commercial filter systems for arsenic removal. Environmental Science & Technology 2011, 45, (17), 7533-7541.
  • Muehe, E. M.; Scheer, L.; Daus, B.; Kappler, A., Fate of arsenic during microbial reduction of biogenic vs. abiogenic As-Fe(III)-mineral co-precipitates. Environmental Science & Technology 2013, 47, 8297−8307.
  • Muehe, E. M.; Kappler, A., Arsenic mobility and toxicity in the environment – a review on biogeochemistry, health and socio-economic effects, remediation and future predictions. Environmental Chemistry 2014, 11, 483–495.
  • Muehe, E. M.; Morin, G.; Scheer, L.; Pape, P. L.; Esteve, I.; Daus, B.; Kappler, A., Arsenic(V) incorporation in vivianite during microbial reduction of arsenic(V)-bearing biogenic Fe(III) (oxyhydr)oxides. Environmental Science and Technology 2016, 50, (5), 2281-2291.
  • Muehe, E. M.; Kappler, A., Biogene Eisenminerale kontrollieren das Umweltverhalten toxischer Metalle. BIOspektrum 2016, 22, (3), 316-318.

Plant Molecular Response to Contaminants

Young rice plants exposed to different concentrations of arsenate (As(V)) and inorganic phosphate (Pi) in their growth medium show reduced shoot (A) and root growth (B). Arsenate elicited diverse and opposite responses of different phosphate transporters in roots and shoots (C), while inorganic phosphate triggered a more shallow and uniform transcriptional response in the tested genes. The data showed that only a restricted set of genes, including PT2, PT3, PT5 and PT13 and two SPX-MFS family members, was particularly responsive to arsenate.

  • Muehe, E. M.; Eisele, J. F.; Daus, B.; Kappler, A.; Harter, K.; Chaban, C., Are rice (Oryza sativa L.) phosphate transporters regulated similarly by phosphate and arsenate? A comprehensive study. Plant Molecular Biology 2014, 85, (3), 301-316.
  • Muehe, E. M.; Kappler, A.; Chaban, C.; Daus, B., Measuring the content and speciation of arsenic in different rice tissues. In Bio-protocols, Ed. 2015; Vol. 5, p e1445.
  • Muehe, E. M.; Kappler, A., Arsenic mobility and toxicity in the environment – a review on biogeochemistry, health and socio-economic effects, remediation and future predictions. Environmental Chemistry 2014, 11, 483–495.