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CHAPTER 2
REVIEW OF LITERATURE
Rocks are aggregates of solid matter that are building blocks of our dynamic planet. They
form the earth’s crust and are the parent materials for soil. The minerals in the rocks
contribute to soil fertility. Soils inherit their colour, texture and composition from the
rocks. There are different types of rocks in the world.
2.1 Types of rocks and their mineral composition
The minerals and ores found in rocks have been essential to all forms of life. The rocks
vary greatly in chemical composition. Silicates are the most common minerals while others
constitute less than 10% of the earth’s crust, the most common being carbonates, oxides,
sulphides and phosphates (Gadd 2007). Based on the mode of formation, rocks are
classified into three types namely igneous rocks, sedimentary rocks and metamorphic
rocks.
2.1.1 Igneous rocks
This group of rocks is formed by the cooling of various kinds of magmas and lavas which
differ widely in their chemical composition. Based on the silica (SiO2) content igneous
rocks are classified into acidic, intermediate, basic and ultra basic types. Feldspars, maphic
minerals and quartz are present in this type of rocks. Igneous rocks containing a high
proportion of quartz (60-75%) are classified as acidic, whereas those containing less than
50% quartz are classified as basic. The common igneous rocks are granite, basalt, diorite,
charnockite, syenite and andesite.
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2.1.2 Sedimentary rocks
These rocks are derived from igneous rocks and are formed by the cementing of
fragmentary rock materials and their products deposited by water in a process known as
diagenesis. There are two main groupings of sedimentary rocks namely, clastic and nonclastic type. Alluvial, glacial and aeolian deposits form the unconsolidated sedimentary
rocks. The common sedimentary rocks are conglomerate, sandstone, argillite, breccia,
chert, shale and limestone.
2.1.3 Metamorphic rocks
These rocks are formed from the igneous or sedimentary rocks by the action of intense heat
and high pressure, chemical fluids or combinations of these resulting in considerable
change in the texture and mineral composition although preserving the overall elemental
composition. The common metamorphic rocks are gneiss from granite, quartzite from
quartz or sandstone, marble from limestone and slate from shale.
2.2 Weathering and its types
The process of breakdown of rocks and their minerals is called weathering. It is a slow and
continuous process that began with the formation of continental crust. Weathering
mobilizes cations and anions that are needed by all life forms. Weathering of rocks
depends on major factors such as mineral composition, time of exposure and climatic
conditions. All the process of weathering, physical, chemical and biological are
interconnected and act simultaneously. There are three distinct types of weathering.
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2.2.1 Physical weathering
Physical weathering occurs as a result of mechanical disintegration of rocks. This type of
weathering does not alter the chemical composition of rocks. Physical weathering is a
process of rock fragmentation due to various physical forces associated with factors such
as fluctuations in temperature, change in pressure, growth of crystals, freezing of water and
frost action.
2.2.1.1 Frost wedging
Frost wedging is a dominant process in high altitude environments. In this process, water
which trickles into the cracks, crevices and pores on the rock during the day, freezes at
night. During freezing the volume of water increases by about 9% which in turn exerts
pressure on the rocks and eventually brings about the mechanical disintegration of rocks
(Goudie et al. 2002).
2.2.1.2 Thermal expansion and contraction
Rocks can be broken apart by changes in temperature. Rocks heat up under the sun during
the day and expand. When the air temperature drops at night, rocks cool and contract (Hall
1999). This cycle causes rock particles to break off and this process is called exfoliation.
Different minerals have different coefficients of thermal expansion, as a result of which
spalling of rocks may occur. This is an important mechanism in desert rocks. Onion peel
weathering is a special case of thermal weathering where the layers of the rock peel off like
an onion, one at a time. This is typical of basaltic rocks.
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2.2.1.3 Pressure release
In the process of pressure release, also known as “unloading”, the overlying materials like
other rocks or glaciers are removed by erosion or denudation. This releases the pressure on
the underlying rocks causing upward expansion which sets up pressure and causes
fractures parallel to the rock surface. Over time, sheets of rock break away from the
exposed rocks along the fractures. Exfoliation due to pressure release is also known as
“sheeting”. Rock bursts in mines and retreat of an overlying glacier are examples of
pressure release mechanism.
2.2.1.4 Crystallization of salts
Saline solutions which seep into pores, cracks and joints in the rocks, evaporate due to high
temperature to form salt crystals which disintegrate the rocks as they grow (Amit et al.
1993). Salts such as sodium sulphate, magnesium sulphate and calcium chloride can
expand upto three times or even more and prove to be most effective in disintegrating
rocks. This is a predominant type of weathering along coastal areas, arid and semiarid
regions.
2.2.2 Chemical weathering
Breakdown of rocks occurs as a result of chemical reactions. During chemical weathering,
changes occur in the mineral composition of rocks whereby primary minerals are
converted into secondary minerals. Water is the central mediator of chemical weathering.
Different chemical reactions which bring about weathering of rocks are described.
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2.2.2.1 Solution
Some of the minerals which are water soluble can be removed in solution. The solvent
action of water is increased in the presence of carbon dioxide and organic acids released
during the decomposition of organic matter. The process of removal of soluble material
from the rocks in solution by percolating water is termed as leaching. Halite (NaCl) and
sylvite (KCl) are highly water soluble while carbonates and sulphates are sparingly soluble.
Weathering of limestone occurs by this process in the presence of CO2.
2.2.2.2 Hydration
Hydration implies the association of water molecules with minerals. In this process certain
minerals take up water, which leads to a change in mineral composition of rocks. The well
known examples of hydration include conversion of anhydrite and hematite to gypsum and
limonite respectively.
CaSO4 + 2H2O
CaSO4.2H2O ;
Fe2O3 + nH2O
Fe2O3.nH2O
(Anhydrite)
(Gypsum)
(Hematite)
(Limonite)
2.2.2.3 Hydrolysis
It is the most important process of chemical weathering. It is a process of exchange
reactions between the bases of the minerals and the hydrogen ions of dissociated water
molecule. Examples of hydrolysis include potash feldspar orthoclase and olivine to
potassium hydroxide and magnesium hydroxide respectively.
KAlSi3O8 + HOH
HKAlSi3O8 + KOH;
MgFeSiO4 +2HOH
(Orthoclase)
(Alumino-silicic acid) (Olivine)
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H2SiO3 + Mg(OH)2 +FeO
(Silicic acid)
2.2.2.4 Carbonation
It is a process by which CO2 is added to minerals to form certain carbonates. Rain water
dissolves some CO2 present in the atmosphere to form carbonic acid which reacts with
several minerals. This process is more effective with minerals containing alkali metals such
as sodium, potassium, calcium and magnesium. An example of carbonation can be
illustrated as follows.
2KAISi3O8 + H2CO3 + H2O
K2CO3 + Al2 Si2O5(OH) 4 + 4SiO2
(Orthoclase)
(Kaoclinite)
2.2.2.5 Oxidation
The process of oxidation involves the chemical union of oxygen atoms with atoms of
metallic elements to form respective oxides. The ferromagnesian minerals such as
pyroxenes, hornblende and olivine rapidly undergo oxidation in the surface conditions,
producing a brown crust consisting largely of oxides of iron. Oxidation of pyrite (FeS2) to
limonite (Fe2O3. nH2O) is a well known example of oxidation.
FeS2 + nO2 + mH2O
FeSO4
(Pyrite)
(Ferrous sulphate) (Ferric sulphate)
Fe2(SO4)3
Fe2O3.nH2O
(Limonite)
2.2.3 Biological weathering
Plants and animals cause biomechanical weathering. The roots of plants loosen the rock
material. Plants growing in a crack can make the crack larger as the roots spread out. This
is known as root-pry. Earthworm, snail and burrowing animals such as rodents also
participate in biological weathering process (Lian bin et al. 2008). Microbes play a key role
in the weathering of major types of rocks, releasing various elements they need as nutrients
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(Calvaruso et al. 2006). Plant roots along with the associated microbes physically disrupt
sheet silicates and thus, exposing new surface area for biochemical weathering (April and
Keller 1990). Biological weathering is influenced by a variety of environmental factors,
such as illumination, humidity, available nutrients and rainfall amount.
2.3 Biogeochemical deterioration mechanisms
Rocks and minerals are known to be chemically susceptible to various biological products
of bacterial metabolism such as protons, organic acids, siderophores, hydroxyl ions,
enzymes and extracellular polysaccharides. Organic acids and chelating molecules play a
significant role in mineral weathering (i) by direct electron transfer they extract nutrients
from mineral particles by adhering to the mineral surfaces (ii) they break or weaken the
metal oxygen bonds and (iii) they chelate cations, thereby they indirectly accelerate
mineral dissolution by creating an imbalance between cations and anions (Welch et al.
2002). For example, gluconic acid, a bacterial metabolite has both acidifying and chelating
functions which induce phosphate solubilization (Kim et al. 2005). EPS affect mineral
stability in three ways, (i) They form complexes with metal ions either at the mineral
surfaces or with metal ions released into solution, (ii) They serve as a nucleation sites for
the formation of secondary minerals and (iii) They retain water at the mineral surfaces
keeping them hydrated (Welch and McPhail 2003). Under acidic conditions Welch et al.
(1999) found that a variety of EPS enhanced the dissolution of plagioclase significantly.
Mineral dissolution due to acidic polysaccharide gels increased by a factor of 100
compared to inorganic controls. Direct silicate precipitation by bacteria via metal sorption
at the cell membrane is also a proposed biogeochemical mechanism (Urrutia and
Beveridge 1994; Konhauser and Ferris 1996). Acidolysis and complexolysis processes can
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be used simultaneously by bacteria in geochemical deterioration of minerals (Uroz et al.
2009).
2.3.1 Acidolysis
Acidolysis is a process which leads to mineral dissolution owing to acidification of the
medium. Production of protons by microorganisms is one of the key factors that influence
mineral stability. Various mineral acids such as nitrous acid, nitric acid, sulphuric acid and
organic acids such as oxalic acid, gluconic acid and citric acid are formed by
microorganisms. The protons associated with these acids decrease the pH of the rock and
induce the release of cations such as iron, potassium and magnesium (Hirsch et al. 1995;
Puente et al. 2004; Uroz et al. 2009). These acids dissolve and etch the mineral matrix with
subsequent weakening of the binding system. As acidity increases below pH 5, the rates of
dissolution of silicate minerals increase by a factor of an (Blum and Lasaga 1988). When
the pH is reduced to 3 or 4, a 10 to 1000-fold increase is observed in the mineral
dissolution rates. At neutral pH, elements such as Fe and Al are relatively insoluble but
when acidity increased, solubility and mobility of Fe and Al is enhanced leading to the
formation of secondary minerals such as aluminosilicates, kaolinite and halloysite
(Banfield et al. 1999). These acids are also capable of chelating cations such as Ca, Al, Si,
Fe, Mn and Mg from minerals forming stable complexes (Schalscha et al. 1967). It has
been shown that biogenic organic acids are more effective than inorganic acids in mineral
mobilisation (Manley and Evans 1986). Among microorganisms fungi are dominant to
weather rocks and minerals (Gehrmann and Krumbein 1994; Becker et al. 1994).
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2.3.2 Chelation
Chelation is a biological process where organisms produce organic substances, known as
chelates that have the ability to decompose minerals and rocks by the removal of metallic
cations. Complex chemical effects occur as a result of chelation. Chelating molecules are
found to increase the dissolution rates of cations by forming strong bonds with cations or
with mineral surfaces (Palmer et al. 1991; Welch et al. 2002; Uroz et al. 2009). The
process of chelation is widely reported for the ability of bacteria to produce siderophores
which have strong affinity for iron. Siderophores are excreted under iron limiting
conditions by various groups of bacteria, such as Pseudomonas, Collimonas and Bacilli
which chelate and take up iron from the rocks in to the cells. Also, some catechol
derivatives produced by Azotobacter and Streptomyces are found to increase the
dissolution of iron containing minerals such as olivine, glauconite, hornblende and goethite
(Page and Huyer 1984; Liermann et al. 2000; Kalinowski et al. 2000). Hydroxamate and
catechol type siderophores are produced by Collimonas species which mobilised iron from
biotite (Uroz et al. 2009). Siderophores also form complexes with number of divalent and
trivalent cations and accelerate the dissolution of minerals such as goetite, hematite and
horneblende (Konhauser 2007). Siderophores also play a key role in the regulation of auxin
level in plants growing in metal contaminated sites. Siderophores complex with toxic
metals, decreasing free metals concentration, thereby attenuating metal inhibiton of auxin
synthesis (Dimkpa et al. 2008). Agrobacterium and Bacillus strains are known to weather
phlogopite via aluminium chelation thereby destabilising the crystal structutre (Leyval and
Berthelin 1989).
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2.3.3 Oxidoreduction
In this process, the reduction or oxidation of a chemical compound entrapped in a complex
structures of rocks, results in instability of the mineral crystal and hence its dissolution.
Bacterial oxidation of elemental sulphur such as pyrite (FeS2) to the corresponding metal
sulphate is an example in which oxidoreduction leads to mineral dissolution and a similar
process was involved in biotite weathering (Uroz et al. 2009). Microorganisms are capable
of removing iron and manganese cations from the mineral lattice of rocks by oxidation
(Braams 1992; de la Torre and Gomez-Alarcon 1994). The rate of oxidation of ferrous iron
released from pyrite due to bacterial action is upto 1 million times faster than inorganic
oxidation rate at low pH (Norstrom and Southam 1997).
2.4. Microorganisms and biological weathering
Microbial processes affect different stages of geochemical cycles leading to mineral
transformations. They are involved in the dissolution of primary and secondary minerals.
Microbial weathering may be aerobic or anaerobic process and may occur in acidic or
alkaline environment (Berthelin 1983). The transfer of biological materials such as fungal
and bacterial spores and other reproductive structures by wind, water and bird droppings
may play an important role in the initial colonisation of rocks. Also, microorganisms may
be entrained within the rocks by various processes such as snowmelt, rainfall and some
aeolian transport (Cockell et al. 2009). Physical properties (eg. porosity) and elemental
composition of the rock (eg. carbon, phosphorus, potassium, sulphur, metal content) may
govern the initial establishment, growth and survival of microbial communities (Gleeson et
al. 2005, 2006). Microbial colonization can dramatically impact both the rates and
mechanisms of silicate weathering both by direct and indirect processes (Banfield et al.
1999).
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2.4.1 Lichens
Lichens are the association between fungus and a photosynthetic partner either green algae
or cyanobacteria. Lichens which dwell on rocks are known as saxicolous species and fall
under distinct groups such as (i) Crustose (ii) Fruticose and (iii) Foliose based on their
mode of attachment to rocks (Jones and Wilson 1985; Carcia-Rowe and Saiz Jimenez
1991). Lichens may be epilithic or endolithic (Bell 1993). Some species are partially
epilithic and partially endolithic (Golubic et al. 1981) while few others may have
chasmoendolithic and euendolithic phases at different stages of colonisation (Ascaso et al.
1995). Weathering of rocks by lichens can be attributed to both physical and chemical
processes. Physical disruption of rocks is caused by hypal penetration (Arino et al. 1997),
contraction and expansion of lichen thallus by microclimatic wetting and drying (Moses
and Smith 1993), incorporation of mineral fragments into the thallus, swelling action of the
organic and inorganic salts produced due to lichen activity. Chemical disruption is due to
the generation of respiratory CO2, excretion of various organic acids and salts which are
found to dissolve minerals and the production of biochemical compounds which chelates
metallic cations. Lichen has been shown to weather rock in situ (Jones et al. 1981) and
Barker and Banfiled found that lichen weathered syenite. Weathering of sandstone basalt,
granitic and calcareous rocks by lichens and their mode of action in weathering of rocks
are well documented (Chen et al. 2000). An experimental study on hornblende granite in
New Jersy, USA, demonstrated a 3 to 4-fold increase in the rate of weathering under lichen
covered surfaces compared to exposed barren rock surfaces (Zambell et al. 2012).
2.4.2 Fungi
Rock colonisation and the distribution of fungal colonies depend on chemical and mineral
composition of rocks and microtopography. Fungal colonies are predominant along the
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cracks and crevices between the rock crystals. Epilithic and endolithic fungal communities
produce osmolytes and carbohydrate polymers in response to desiccation which prolong
the water residence time, increasing the duration of chemical reactions causing silicate
weathering. These biophysical and biochemical reactions results in the expansion of rocks,
which eventually cause spalling of surface layers from the weakened rocks below
(Gaylarde et al. 2004). Many rock inhabiting fungi are melanised. Melanin pigmentation
confers extra-mechanical strength to the hyphae to penetrate the rock surface and crevices
(Dornieden et al. 1997; Sterflinger and Krumbein 1997) and also, offers protection from
metal toxicity (Gadd 1993). Fungi have been reported from a wide range of rock types,
including rocks from extreme environments (Staley et al. 1983; Nienow and Fridman 1993;
Sterflinger 2000; Etienne and Dupont 2002; Gorbushina 2007).
2.4.3 Bacteria
Bacteria produce a wide range of low molecular weight organic exudates such as oxalates
and citrates (Jones 1998; Neaman et al. 2005). In an experimental study conducted by
Puente et al. (2004), fluorescent pseudomonads and Bacilli were found to weather igneous
rocks, limestone and marble. Root and mycorrhiza associated bacteria are involved in the
weathering of biotite and anorthite (Balgoh et al. 2008, Calvaruso et al. 2006). Bacteria
promote the weathering of iron and magnesium containing silicates such as biotite by
producing siderophores (Frey-Klett et al. 2007). Mineral dissolution studies with cultures
of bacteria and fungi showed a dramatic increase in the dissolution rates of feldspar,
biotite, quartz, apatite and other minerals (Ullman et al. 1996; Barker et al. 1997; Berthelin
and Belgy 1979; Thorseth et al. 1995; Callot et al. 1987; Paris et al. 1996).
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2.5 Types of habitats of rock bacteria
Rocks offer a variety of microhabitats to microbes. Although they might appear to be
similar, each microhabitat has different environment thus harbouring different microbial
colonists and hence to differentiate between them is biologically important. The interior of
the rocks received meticulous attention as a potential habitat for microorganisms in
extreme deserts of the world because of the ameliorated environmental conditions found in
this ecological niche compared with their surfaces (Friedmann and Kibler 1980). The
refugium that rock interiors afford as an escape from environmental extremes such as
temperature, UV radiation and desiccation, has made them the subject of interest as
possible locations for life on early earth (Westall and Folk 2003). These microbial
communities influence weathering (Warscheid and Krumbein 1994), elemental cycling and
nutrient gradients (Friedmann 1982).
2.5.1 Epilithic habitat
The surface of the rocks provides an epilithic habitat for a diverse microorganism and
provides a stable environment for biofilm development. These rock surface biofilms forms
desert varnishes and crusts in hot deserts of the world (Kurtz and Netoff 2001; Perry et al.
2003). Lichen, cyanobacteria, gram positive bacteria and actinomycete epilithis are
reported from a number of locations (Gold and Bliss 1995; Quesada et al. 1999; Dickson
2000; Palmer et al. 1986; Eppard et al. 1996). Epilithic microorganisms are found to
colonise any rock surface where adequate nutrients and water are available.
2.5.2 Hypolithic habitat
Hypolithic organisms are found on the underside of the rock which provides a habitat for
both photosynthetic and non-photosynthetic microbes (Smith et al. 2000). Most hypolithis
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are repoted under quartz-dominated rocks which are translucent for the light to penetrate
directly through the rock which is a necessary requirement for phototrophs (Broady1981;
Schlesinger et al. 2003). This habitat was found to be dominated by Gloecapsa and
Chroococcidiopsis (Cockell and Stokes 2004).
2.5.3 Endolithic habitat
Endolithic organisms are those which live inside the rocks and they have great advantage
over other type of rock dwellers because this microenvironment protects the organisms
from various climatic disturbances. For example, the temperature within the interior of the
rocks are higher than air temperature by upto 10°C (Cockell et al. 2003), the rain water
gets trapped in the pores providing water for the organisms where the surface water dries
and the interior of the rocks offers protection against UV radiation (Cockell et al. 2002).
Based on the microenvironment, endolithic habitats are further classified as
cryptoendolithic, chasmoendolithic and euendolithic habitats.
2.5.3.1 Cryptoendolithic habitat
The cryptoendolithic organisms live within the pores of the rocks, invading the pore spaces
to reach the interior of the rocks. The pore spaces must be interconnected to allow them to
spread within the rock matrix (Saiz-jimenez et al. 1990). Increase in the porosity of the
rock allows the microorganisms to move within the rock either by growth along the surface
or by water transport (Cockell et al. 2002). These interconnected pores provide a suitable
habitat for a wide variety of heterotrophic microorganisms, providing protection from
environmental stresses. The best characterized photosynthetic cryptoendolithic habitats are
sedimentary rocks which are translucent and porous such as those associated with
sandstones and limestones (Wessels and Del 1995).
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2.5.3.2 Chasmoendolithic habitat
The chasmoendolithic organisms live within the cracks and fissures in the rocks. Unlike
the cryptoendolithic habitat, the chasmoendolithic habitats can potentially be formed in any
of the substrate rocks and they need not essentially be translucent for the penetration of
sunlight, because light penetrates directly into the cracks on the rock substrate. Shattered
limestones are found to harbour cyanobacterial chasmoendolthic communities (Cockell et
al. 2004).
2.5.3.3 Euendolithic habitat
The euendolithic organisms live deep into the rock by actively boring the rock substrate
and the most common substrates for euendoliths being carbonate rocks. Organic acids
produced by the microbes help them to bore into the substrate carbonate rocks by readily
dissolving them. Euendolithic borings were also preferentially found on the margins of
basaltic glasses, where access to substrate and nutrients are available (Fisk et al. 1998).
2.6 Diversity of rock-weathering bacteria
Cultivable heterotrophic bacteria such as Arthrobacter, Bacillus, Micrococcus,
Paenibacillus, Pseudomonas and Rhodococcus have been identified as the most common
rock inhabiting microorganisms (Gurtner et al. 2000; Gorbushina et al. 2002; 2004;
Heyrman et al. 2005; Ortega-Morales et al. 2005). Bacterial strains Burkholderia glathei
and Burkholderia fungorum were reported for their ability to weather complex minerals
and rocks such as biotite, basalt or granite (Uroz et al. 2007; Wu et al. 2007, 2008).
Thorseth et al. (1992) hypothesized that when rocks are exposed to sufficient light for
photosynthesis, cyanobacterial growth could create local changes in pH that cause
biomineralization. This may be attributed by their ability to photosynthesize and fix
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atmospheric nitrogen. Various cyanobacterial species such as Anabaena, Calothrix,
Nostoc, Prochlorococcus and Stigonema have been reported on rock surfaces (Gorbushina
and Broughton, 2009; Herrera et al. 2008; Olsson-Francis et al. 2010; Kelly et al. 2011).
Some chemical components of rocks can be directly utilized by bacteria as energy source.
Thiobacillus species oxidize the pyrite present in sandstones (Krumbein 1972). Clarke et
al. (2011) found Shewanella oneidensis, a member of rock-dwelling bacteria used iron as a
source of energy and with special type of proteins, transported electrons outside the cell
into iron. Bacillus mucilaginosus is found to dissolve illite, kaolinite and chlorite
preferentially than other silicate minerals and produce pyrophyllite and hornblende (Binbin
and Lian Bin 2010). Sulfur and nitrifying bacteria were frequently reported from weathered
rock surfaces (Bock 1987; Bock and Sand 1993; Warscheid and Braams 2000).
2.7 Genetics of rock-weathering bacteria
Bacteria are known to play a role in rock weathering, but the genomics of biological rock
weathering is yet to be explored. Little is known about the precise molecular mechanisms
and the genes involved. Mason et al. (2009) confirmed the presence of nitrogen fixation
genes in basalt. Mason et al. (2010) also analyzed igneous rocks of ocean crust using
various techniques such as denaturing gradient gel electrophoresis, sequencing and
terminal restriction fragment length polymorphism, cloning and sequencing and functional
gene microarray analysis and found that gabbroic microbial community were found to be
closely related to bacteria from hydrocarbon-dominated environment. Using a microarray
for metabolic genes, functional gene diversity in the gabbroic samples was analyzed.
Genes coding for anaerobic respirations such as nitrate reduction, sulfate reduction and
metal reduction, as well as genes involved in carbon fixation, nitrogen fixation and
ammonium-oxidation were identified. Various functional genes coding for methane
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production (mcr), methane oxidation (pmo and mmo), carbon fixation (acsA, FTHFS,
rbcL, rbcS), denrification (narG, nirK, norB), sulphate reduction (dsrA, dsrB) and metal
reduction (iron) indicates that bacterial communities in these gabbroic rock samples have
immense potential and can be exploited for diverse applications. Olsson-Fransis et al.
(2010) used microarray technique to determine the genes involved in the sequestration of
iron in Cupriavidus metallidurans CH34. In Bacillus mucilaginosus using two-dimensional
electrophoresis and tandem mass spectrometry, Xiao et al. (2012) found that bacterial
secreted proteins associated with K-bearing mineral crystal by means of electron transfer.
Polysaccharides and other extracellular polymers absorb mineral elements in solution and
achieve dissolution to acquire inorganic nutrients.
2.8 Role of rock-weathering rhizobacteria in plant growth-promotion
Microbial stimulation of mineral dissolution directly affects the fertility of agricultural soil
(Banfield et al. 1999). During primary colonisation of rock substrates by plants, mineral
weathering is strongly accelerated under plant roots (Bashan et al. 2002; Milton 2006;
Uroz et al. 2007) and enhanced by the association of rhizoplane microbiota (CarrilloGracia et al. 1999). Plants participate in rock weathering by secreting a combination of
sugars, organic acids and amino acids in root exudates there by attracting bacteria (Lynch
and Whipps 1990). Rhizobacteria thriving on rocks in turn play an indispensible role in
maintaining a continuous supply of inorganic nutrients for plants (Chang and Li 1998;
Hinsinger et al. 1992). Different plants support different levels of colonisation of bacteria.
Presence of cristobolite and calcite in plant bearing rocks, not found in the parent bed rock
indicates biomineralisation due to the rhizobacteria of plants (Bashan et al. 2002).
Mycorrhiza associated bacteria in the root environment are significant in mineral
weathering and plant nutrition (Balogh-Brunstad et al. 2008; Koele et al. 2009).
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Fluorescent pseudomonads and bacilli isolated from the rhizospheres of Ficus palmeri and
cacti species are shown to enhance weathering of volcanic rocks by the production of
volatile and non-volatile organic acids. These bacteria were also able to promote the
growth of cactus seedlings by releasing significant amounts of nutrients from rocks. These
strains were individually inoculated onto seeds of the giant cardon cactus. After 12 months,
where plants were irrigated only with micronutrients solution lacking N and P, significant
growth promotion was observed, including increase in dry weight, volume, height of plants
and size of main root. Uninoculated control plants either died or were significantly
dwarfed. Results suggest that microorganisms may serve as plant growth-promoting
bacteria (Puente et al. 2004; 2009). Calvaruso et al. 2006 demonstrated that B. glathei
strain PML1(12) when inoculated with pine seedlings grown in a mixture of biotite and
quartz, significantly enhanced the release of potassium and magnesium compared to the
uninoculated control. Fluoroapatite and labradorite plagioclase minerals were significantly
more weathered in the rhizosphere zone than in a zone where roots were excluded. This
supports the fact that rhizobacteria participate in the release of key nutrients from primary
minerals. Cochran and Berner (1996) and Moulton et al. (2000) found that much higher
weathering rates are observed when the basalt rock was colonised by higher plants,
compared with that of bare rock or rock covered with lichens. Hinsinger et al. (2001)
studied the weathering of a basalt rock in a microcosm and found that the planted system
leads to 2 to 10-fold increased dissolution rates for most elements (Ca, Mg, Si), compared
with unplanted systems. Barak et al. (1983) demonstrated that finely ground basalt and
basaltic tuff helped in the micronutrient (Fe) fertilization of peanuts grown in calcareous
soils. Koele et al. (2009) found that pine biomass was significantly improved by
coinoculating Scleroderma citrinum with a mineral weathering Collimonas strain
compared with uninoculated control. Similarly, Carrillo et al. (2002) demonstrated that the
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plant growth in desert soil is enhanced by inoculation of a cardon seedling with a specific
strain of Azospirillum brasilense.
2.8.1 Phosphate solubilization
Phosphorus is an important macronutrient essential for plant growth and development
(Ehrlich 1990). An important limiting factor to food production in many agricultural soils
is the deficiency of plant-available phosphorus. Of total soil phosphorus, only 1 to 5% of
phosphorus is in a soluble and plant-available form (Molla and Chowdhury 1984). Mineral
rocks contain large reserves of insoluble apatite, the primary phosphorus bearing mineral in
phosphatic rock include fluorapatite, hydroxyapatite, carbonatehydroxyapatite and
francolite (Van straaten 2002). Root colonising bacteria from rock-weathering desert plants
were able to produce volatile and non-volatile organic acids which reduced the pH of the
rock and enhanced phosphate solubilisation. Various strains of rock dwelling microbial
communities have been reported for their ability to dissolve phosphate from rocks such as
Pseudomonas, Bacillus, Citrobacter and Enterobacter (Toro et al. 1997; Carrillo et al.
2002; Puente et al. 2004). Granitic rock was found to support bacteria which closely
resembled Gluconobacter oxydans with genes that code for histidine acid phosphatase
(HAP), an enzyme involved in the mineralization of phytate which is a rich organic
phosphorus compound (Bates 2011). Therefore, exploitation of phosphate solubilizing
bacteria in agriculture has enormous potential for making use of natural reserves of
phosphate rocks.
2.8.2 Nitrogen fixation
Microorganisms play key roles in nutrient cycling and thus have important effects on soil
development and plant establishment. Microbial nitrogen fixation is of particular interest,
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since the availability of nitrogen species is one of the key limitations for plants growing on
rocks. Analysis of metagabbros rock revealed that nitrogen concentration are low and
hence, nitrogen fixation in this environment would be paramount (Busigny et al. 2005).
Nitrifying bacteria solubilise calcium carbonate and participates in weathering of limestone
(Jaton 1972). Lichen associated bacterial communities from granitic rocks closely
resembled nitrogen fixing taxa such as Frankia, Beijerinckia, Bradyrhizobium,
Azospirillum, Pseudomonas stutzeri, Acinetobacter, Burkholderia, Gluconobacter and
Rhodospirillum (Torre et al. 2003; Bates 2010) suggesting that such rock dwelling
microbial communities can be exploited for use in agriculture.
2.8.3 Supply of other essential nutrients
Weathering of rocks by microorganisms results in the mobilisation and redistribution of
essential nutrients and metals such as S, Na, K, Ca, Fe, Cu, Zn, Co and Ni which are
essential for plant growth (Morley et al. 1996). Puente et al. (2004) showed that Bacillus
and Pseudomonas isolated from the rhizoplane of rock-weathering plants were able to
release significant amounts of useful elements such as Mg, Mn, Fe, Cu, Zn and K.
Nitrifying bacteria also participate in the weathering of serpentinized ultrabasic rocks there
by releasing various essential minerals (Bertherlin et al. 1985). Rhizoplane bacteria of
lithotrophic plants participate in the supply of inorganic nutrients, organic acids (Lynch
and Whipps 1990).
2.8.4 Tolerance to adverse environmental conditions
Rock inhabiting bacteria not only help plants by nutrient mobilization but also support
plants to withstand adverse conditions of salinity, pH, heavy metals, extreme temperatures
and drought (Cockell 2009). Pseudomonas and Bacillus persisting in the roots of cacti
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growing on rocks were found to be salt-tolerant (3% NaCl), drought resistant and thermo
tolerant, surviving the long summer at elevated temperatures over 60°C (Puente et al.
2004). Several rDNA sequences and cultured examples of Deinococcus-like organisms
were also isolated from sandstone rocks from Antartica (Hirsch et al. 1988, Siebert and
Hirsch 1988; de la Torre et al. 2003). These bacteria are known for their ability to tolerate
large amounts of ionising radiation-induced damage to their DNA. However, studies have
suggested that this ability may be an adaptation to repair DNA damage induced by
desiccation (Mattimore and Battista 1996). Rocks also contain numerous biologically
detrimental transition metals at low concentration and the organisms growing in these rock
environments should be tolerant if they have to survive and participate in rock weathering.
They include Cr, Ni, Cu, V and Co (Carmichael 1964; Walsh and Clarke 1982). Nonessential and potentially toxic metals such as Cs, Al, Cd, Hg and Pb may also be mobilized
from rock mineral (Gadd 2001, 2001; Morley et al. 1996). Some rocks contain high
abundances of minerals enriched in toxic elements such as Ar, Cd, Hg and U.
Microorganisms react to high metal concentration by the production of extracellular
polymers that bind and effectively immobilize the compound. Microbes immobilize
uranium by intracellular and extracellular precipitation of secondary minerals (Macaskie et
al. 1997; Jeong et al. 1997). In other cases, microorganisms convert them into less toxic
form and secrete them from the cells in the case of arsenic or completely volatilize the
toxic element in the case of mercury by forming methyl mercury compounds (Silver 1997).
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