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Microbe-mineral interactions in soil: Investigation of biogenic chelators, microenvironments and weathering processes
Stockholm University, Faculty of Science, Department of Geological Sciences.
2015 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The interplay between geology and biology has shaped the Earth during billions of years. Microbe-mineral interactions are prime examples of this interplay and underscore the importance of microorganisms in making Earth a suitable environment for all forms of life. The present thesis takes an interdisciplinary approach to obtain an integrated understanding of microbe-mineral interactions. More specifically it addresses how the composition and distribution of biogenic weathering agents (siderophores) differ with regard to soil horizon and mineral type in situ, what siderophore type soil microorganisms produces under laboratory conditions, what role microbial surface attachment plays in mineral weathering reactions and what central roles and applications siderophores have in the environment.

Podzol, the third most abundant soil in Europe, and most abundant in Scandinavia, was chosen for a field experiment, where three minerals (apatite, biotite and oligoclase) were inserted in the organic, eluvial and upper illuvial soil horizons. The study started with an investigation of the siderophore composition in the bulk soil profile and on the mineral surfaces (paper I), which was followed by a study of the siderophore producing capabilities of microorganisms isolated from the soil profile under laboratory conditions (paper II). Subsequently, a study was done on the impact of microbial surface attachment on biotite dissolution (paper III). Finally, the roles of siderophores in nature and their potential applications were reviewed (paper IV).

The major findings were that the concentration of hydroxamate siderophores in the soil attached to the mineral surfaces was greater than those in the surrounding bulk soil, indicating that the minerals stimulate the microbial communities attached to their surfaces to produce more siderophores than the microorganisms in the bulk soil. Each mineral had a unique assemblage of hydroxamate siderophores, that makes the mineral type one of the main factors affecting siderophore composition in the natural environment. Siderophore production varied between the microbial species originating from different soil horizons, suggesting that the metabolic properties of microbes in deep soil horizons function differently from those at upper soil horizons. Microbial surface attachment enhanced the biotite dissolution, showing that attached microbes has a greater influence on weathering reactions in soil than planktonic populations. In conclusion, our findings reflected that the complicated relationship between microorganisms and mineral surfaces reinforces the central theme of biogeochemistry that the mineral controls the biological activity in the natural environments. However, the importance of these relationships to the biogeochemical systems requires further investigation.

Place, publisher, year, edition, pages
Stockholm: Department of Geological Sciences, Stockholm University , 2015.
Keyword [en]
Podzol, Biotite, Apatite, Oligoclase, Microbial attachment, Siderophores, Soil microorganisms
National Category
Earth and Related Environmental Sciences
Research subject
Geochemistry
Identifiers
URN: urn:nbn:se:su:diva-115250ISBN: 978-91-7649-135-5 (print)OAI: oai:DiVA.org:su-115250DiVA: diva2:796173
Public defence
2015-05-11, Nordenskiöldsalen, Geovetenskapens hus, Svante Arrhenius väg 12, Stockholm, 13:00 (English)
Opponent
Supervisors
Note

At the time of the doctoral defense, the following papers were unpublished and had a status as follows: Paper 2: In press. Paper 3: In press.

 

Available from: 2015-04-20 Created: 2015-03-18 Last updated: 2016-02-03Bibliographically approved
List of papers
1. The effect of soil horizon and mineral type on the distribution of siderophores in soil
Open this publication in new window or tab >>The effect of soil horizon and mineral type on the distribution of siderophores in soil
2014 (English)In: Geochimica et Cosmochimica Acta, ISSN 0016-7037, E-ISSN 1872-9533, Vol. 131, 184-195 p.Article in journal (Refereed) Published
Abstract [en]

Iron is a key component of the chemical architecture of the biosphere. Due to the low bioavailability of iron in the environment, microorganisms have developed specific uptake strategies like production of siderophores. Siderophores are operationally defined as low-molecular-mass biogenic Fe(III)-binding compounds, that can increase the bioavailability of iron by promoting the dissolution of iron-bearing minerals. In the present study, we investigated the composition of dissolved and adsorbed siderophores of the hydroxamate family in the soil horizons of podzol and the effect of specific mineral types on siderophores. Three polished mineral specimens of 3 cm x 4 cm x 3 mm (apatite, biotite and oligioclase) were inserted in the soil horizons (O (organic), E (eluvial) and B (upper illuvial)). After two years, soil samples were collected from both the bulk soil of the whole profile and from the soil attached to the mineral surfaces. The concentration of ten different fungal tri-hydroxamates within ferrichromes, fusigen and coprogens families, and five bacterial hydroxamates within the ferrioxamine family were detected. All hydroxamate types were determined in both soil water (dissolved) and soil methanol (adsorbed) extracts along the whole soil profile by high-performance liquid chromatography coupled to electrospray ionization mass spectrometry (HPLC-ESI-MS); hence, the study is the most extensive of its kind. We found that coprogens and fusigen were present in much higher concentrations in bulk soil than were ferrioxamines and ferrichromes. On the other hand, the presence of the polished mineral completely altered the distribution of siderophores. In addition, each mineral had a unique interaction with the dissolved and adsorbed hydroxamates in the different soil horizons. Thus siderophore composition in the soil environment is controlled by the chemical, physical and biological characteristics of each soil horizon and also by the available mineral types.

National Category
Earth and Related Environmental Sciences
Identifiers
urn:nbn:se:su:diva-102946 (URN)10.1016/j.gca.2014.01.031 (DOI)000333330100013 ()
Note

AuthorCount:2;

Available from: 2014-04-30 Created: 2014-04-25 Last updated: 2017-12-05Bibliographically approved
2. Siderophore Production by Microorganisms Isolated From a Podzol Soil Profile
Open this publication in new window or tab >>Siderophore Production by Microorganisms Isolated From a Podzol Soil Profile
2015 (English)In: Geomicrobiology Journal, ISSN 0149-0451, E-ISSN 1521-0529, Vol. 32, no 5, 397-411 p.Article in journal (Refereed) Published
Abstract [en]

Siderophore-producing bacteria/actinobacteria and fungi were isolated from O- (organic), E- (eluvial), B- (upper illuvial), and C- (parent material) horizons of podzol soil. Siderophores were isolated and hydroxamate type siderophores were detected and quantitated by high-performance liquid chromatography coupled to electrospray ionization mass spectrometry. The molecular identification of siderophore-producing isolates showed that there was a high diversity of fungal and bacterial/actinobacterial species throughout the soil profile. The isolated bacteria/actinobacteria showed different abilities in the production of ferrioxamines (E, B, G and D). Moreover, the isolated fungal species showed great variety in the production of ferrichromes, coprogens and fusarinines.

Keyword
bacteria, fungi, hydroxamates
National Category
Earth and Related Environmental Sciences
Research subject
Geochemistry
Identifiers
urn:nbn:se:su:diva-114824 (URN)10.1080/01490451.2014.925011 (DOI)000354619500001 ()
Available from: 2015-03-11 Created: 2015-03-11 Last updated: 2017-04-24Bibliographically approved
3. Microbe-mineral interactions: The impact of surface attachment on mineral weathering and element selectivity by microorganisms
Open this publication in new window or tab >>Microbe-mineral interactions: The impact of surface attachment on mineral weathering and element selectivity by microorganisms
2015 (English)In: Chemical Geology, ISSN 0009-2541, E-ISSN 1872-6836, Vol. 403, 13-23 p.Article in journal (Refereed) Published
Abstract [en]

One of the major gaps within the field of biogeochemistry is the lack of a detailed and deep understanding of the mechanismbehind the microbial inducement of mineral dissolution. The association of microorganisms with the mineral surfaces is an important issue for understanding processes like mineral weathering, biomineralization, bioremediation and biofouling. The present study aims to investigate the performance of attached and unattached soil fungal and bacterial species in biotite weathering and in the selectivity of elements from biotite. Sterilized microplate devices were filled with biotite (>2 mm) followed by an iron limited liquid growth medium and were inoculated separately with six different microbial species isolated from podzol soil: Erwinia amylovora, Pseudomonas stutzeri, Pseudomonas mendocina, Streptomyces pilosus, Neurospora crassa and Penicillium melinii. The experiment was designed in two set-ups: 1) attached form, in which the microorganisms were inoculated directly to the biotite surface, and 2) unattached form, in which 0.4 mu m PET track etched devices were used to separate the microbial cells from the biotite surface. Our findings indicate that the surface attached microorganisms led to a greater dissolution of elements from biotite than the unattached microorganisms that was evidenced by 1) higher dissolution of Fe, Al and Si, 2) greater decrease in pH of the liquid growth medium, and 3) relatively higher production of siderophores. Furthermore, there was no significant difference in the capability of element selectivity between the attached and unattached microbial forms. The biotite dissolution was promoted initially by complexation processes and later by acidification processes for most of the attached and unattached microorganisms. Thus, we conclude that despite the mineral dissolution induced by microbial attachment on the mineral surface, the element composition of the biotite and nutritional need of the microorganisms were the main factors affecting the element selectivity.

Keyword
Acidification, Biotite, Bacteria, Complexation, Fungi, Siderophores
National Category
Earth and Related Environmental Sciences
Research subject
Geochemistry
Identifiers
urn:nbn:se:su:diva-117771 (URN)10.1016/j.chemgeo.2015.03.009 (DOI)000353832800002 ()
Available from: 2015-06-05 Created: 2015-06-01 Last updated: 2017-12-04Bibliographically approved
4. Siderophores in environmental research: roles and applications
Open this publication in new window or tab >>Siderophores in environmental research: roles and applications
2014 (English)In: Microbial Biotechnology, ISSN 1751-7907, E-ISSN 1751-7915, Vol. 7, no 3, 196-208 p.Article, review/survey (Refereed) Published
Abstract [en]

Siderophores are organic compounds with low molecular masses that are produced by microorganisms and plants growing under low iron conditions. The primary function of these compounds is to chelate the ferric iron [Fe(III)] from different terrestrial and aquatic habitats and thereby make it available for microbial and plant cells. Siderophores have received much attention in recent years because of their potential roles and applications in various areas of environmental research. Their significance in these applications is because siderophores have the ability to bind a variety of metals in addition to iron, and they have a wide range of chemical structures and specific properties. For instance, siderophores function as biocontrols, biosensors, and bioremediation and chelation agents, in addition to their important role in weathering soil minerals and enhancing plant growth. The aim of this literature review is to outline and discuss the important roles and functions of siderophores in different environmental habitats and emphasize the significant roles that these small organic molecules could play in applied environmental processes.

National Category
Geology
Identifiers
urn:nbn:se:su:diva-104143 (URN)10.1111/1751-7915.12117 (DOI)000333969900002 ()
Note

AuthorCount:2;

Available from: 2014-06-09 Created: 2014-06-03 Last updated: 2017-12-05Bibliographically approved

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