Microbes and Land Use Change

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Introduction

Land use change refers to anthropogenic alterations of ecosystems. While ecosystems themselves are naturally dynamic units, stresses can push them so that they gain new functions. Microbial communities are part of this system and undergo similar changes. Human’s have had significant effects on many ecosystems and have subsequently altered their ecosystem function and community structure. This is accomplished through the alteration of biological, chemical, and physical factors. Two common examples of land use change are agriculture and the creation of brownfields and polluted sites. In both of these cases, they are affected by influxes of nutrients and pollutants, changing hydrology, alterations of soil architecture, and biological interactions resulting from flora. Essential microbial processes that are critical to this condition with regards to the case studies are decomposition, lithotropy/respiration, nitrification, and denitrification.

Physical factors

Soil structure

Land use changes have many different effects on microbial communities and their habitats. One key effect is through soil structure. Soil structure is the result of many years of natural factors and may have developed particular horizons formative of the ecosystem. Soil horizons may be drastically altered as a result of new land use regimes. In agricultural systems, plowing causes the creation of a defined plow layer (Ap) (1). Soil architecture can also be affected by excessive compaction, which reduces pore size and can limit the permeability of water, gas exchange, and root penetration, all of which have important consequences for microbes (2). Excess soil management, especially from agriculture and resource extraction, can break up this internal organization, resulting in erosion (1).


Hydrology

Hydrological regime shifts can also be associated with land use changes. In addition to soil permeability effects as mentioned above, land use changes may require that streams or rivers may be diverted or channelized, which may affect the hydrology of areas fed by these streams (3). Land use changes may exacerbate flood pulses, change flood intervals, or create new flood plains through the conversions of wetlands or by changing the flow of rivers (4). These hydrology changes resulting from land use change can also impact oxygen levels of the soil, as ecosystems like wetlands are characterized by oxygen poor soils resulting from constant saturation (5), and will affect microbial habitats through the creation or reduction of floodplain conditions. Additionally, soil moisture has an effect on temperature because the high heat capacity of water (6).

Chemical Factors

The chemical effects of land use changes have a huge importance with regard to microbial habitat. Nutrient content of the soil may be saturated or depleted through differing land use-related activities and can affect microbial metabolism, especially through alterations of the C/N ratio (7). Soil management practices can deplete soil organic matter, especially in agriculture. Increased tillage enhances soil O2 content and accelerates the breakdown of soil organic matter (1). Additionally, fertilization and other soil amendment practices may skew nutrient concentrations and ratios, resulting in different mineralization and immobilization rates. This will also have an effect on microbial community composition, as different microbes may have adaptations to different nutrient levels or fertilizer types. For example, soils with poultry litter amendments had higher bacterial diversity than those that were fertilized with inorganic fertilizers (13). Many anthropogenic processes or input from more developed areas can increase the soil content of heavy metals, hydrocarbons, or various other pollutants beyond their natural variation (8). Additional additives that change the pH from the soil can alter the availability of labile forms of nutrients and heavy metals. For example, at lower pHs, aluminium ions are more freely available while phosphorus is complexed by soil particles (9). Nutrients and pollutants in mobile forms can also be leached through erosion processes resulting from overworked soils (1).

Biological Factors

The planting of new or different species of plants as part of a land use change will have an effect on microbes in the context of land use change. The use of mycorrhizal inoculants or introducing crops that form mutualisms with microbial symbionts, such as legumes, can introduce alien species of microbe into the soil. These new species may outcompete the native microbiota or alter the community dynamics. Plants themselves will also compete for nutrients against microbes (21). Additionally, the planting of allelopathic crops may inhibit microbial activity through the exudation of allelochemicals (22).


Microbial communities: Case Studies

Agriculture

Agriculture and forestry have similar types of effects in that these land conversions revolve mainly around direct resource utilization. The ecosystems typically converted to agriculture are either grasslands or slash and burn, which involves the burning and chopping down of trees. Studies of converted grasslands have determined through PFLA [1], Biolog [2], and hybridization probes [3] that most species in cultivated landscapes are Gram-negative, specifically Proteobacteria, Cytophaga-flavobacterium, and acidiobacteria, with little to no archaea (7, 11). In terms of conversions from forests, microbial community structure is dominated predominately by acidiobacteria and proteobacteria (12). In many areas, such as Illinois and North Carolina, wetlands were converted to agriculture through drainage. This transition results in increased percentage of proteobacteria to acidobacteria. Some particular species of bacteria that increased post agricultural conversion include beta-proteobacteria (30). With forest to agriculture conversions, fungal community composition shifts from a mainly Basidiomycete dominated community to an Ascomycete dominated community. These shifts were correlated to changes in phosphorus availability from these land regimes (29). The Glomus genus of fungi was dominant in terms of arbuscular mycorrhizal fungi in both grassland and forest conversions(14). Ectomycorrhizal fungal diversity is often reduced in these conversions as well (28).


Microbial community diversity at individual plots in cultivated areas may drop depending on variation in environmental factors, such as nutrient availability and pH (12). In Steenwerth et al., comparisons between agricultural and grassland soils, microbial species richness was found to decrease (7), while Rodriges et al. found that conversion of the Amazon to cultivation results in an increase of microbial diversity (10). Jesus et al. and Hartman et al. both confirm that changes in microbial community structure is moreso a function of pH and other factors (12, 30). Particular ecosystems are more effected by particular changes. Wetlands, for example, are more strongly affected by pH than they are by soil carbon or nutrient inputs (30). Microbial community structure does homogenize at greater spatial scales, however (12). This can be attributed to the selective pressures resulting from agricultural methods, such as tillage and inorganic fertilizers, applied over larger scales as a monoculture. There are specific populations of acidiobacteria and gamma-proteobacteria that correspond with inorganic fertilizers, explaining why diversity is reduced overall (13). With regards to fungi, arbuscular mycorrhizal species diversity also declined with shifts to more generalist species that reproduced via spores, indicating a shift to r-selected characteristics in response to these new conditions (14). The homogeneous structure of these communities means that it possess less functional diversity and lower resilience to disturbances (7).

An Urban Brownfield

Brownfields/Polluted Areas

A consequence of urbanization and industrialization is the pollution of various areas through contaminants such as heavy metals and petroleum-based substrates. The same applies to heavy metals, and can even be found concurrently with petroleum substrates at sites (15). The microbes present depend upon the pollutants in question. In arsenic and cadmium contaminated soils, for example, fungi and proteobacteria appeared tolerant at the expense of other microbial species (16), while areas with zinc and mercury pollution were found to have more members of Acidiobacteria, such as Acidithiobacillus and Thiothrix (17). Fungal genera that can withstand heavy metal pollution include Geomyces, Pecilomyces, and Mortierella (18), and archaeal phyla include Crenarchaeota (19). In petroleum contaminated soils, one can find Proteobacteria (Gammaproteobacteira, Epsilonproteobacteria) and archaeal phyla (Crenarchaeota) (20).


Microbial community structure also appears to homogenize in these more extreme environments. In Nordgren, Baath, and Soderstrom, the diversity of fungal species decreased as the heavy metal gradient approached its source (18). Similarly, the diversity of petroleum microbes also decreased as conditions were exacerbated. The tolerant microbes are not only able to withstand these conditions but may even exacerbate conditions to limit competition. In Linton, Shotbolt, and Thomas, it was observed that surviving bacterial species in the highest concentration of heavy metals were related to acidophilic species that can oxidize iron and sulfur, reducing the pH and increasing the potency of these heavy metals (17). Similar characteristics can be found with species that can withstand high concentrations of petroleum (20).

Microbial processes

Decomposition

Decomposition is an important microbial process that is affected by conversions of land into agriculture and petroleum pollution. On the whole, there is a net loss in soil organic C in conversion to agriculture. The quality of the litter that agricultural crops will produce may not be equivalent to that of native vegetation and may be incorporated into microbial biomass too quickly if the C:N ratio is lower or may stick around for longer and accumulate as organic matter if the ratio is high (1, 13). Decomposition may also affect the availability of other nutrients, as easily decomposed organic matter will liberate much needed nitrogen and phosphorus for microbial biomass and metabolism (1). Decomposition rates are often higher because reductions of litter, over or understory cover results in a higher soil temperature that stimulates microbial activity. This is amplified by tillage, which increases the soil oxygen content and also increases decomposition (23). Decomposition is also important for microbes impacted by petroleum pollution because those that are adapted can use the hydrocarbons as a carbon substrate (20).

Diagram of decomposition, using compost as an example

Nitrification

Nitrification is one of the major processes that can be affected by land use changes. In agriculture, nitrogen amendments and fertilizers are added to the soil, meaning that microbes are rarely nitrogen deficient. However, since microbes receive an excess of nitrogen, they may further mineralize inorganic forms and convert them to nitrate, which is much more motile. Nitrate can leach from the soil via erosion and can result in nitrogen losses (24).

Denitrification

Denitrification may also contribute to fertility loss. If agricultural soils become saturated and the conditions become anoxic, then available nitrates may be converted by denitrifying bacteria to a gaseous form. Denitrifiers leftover from converted landscapes, such as wetlands, are adapted to the new conditions of the land regime change and may become more sensitive to specific conditions, such as heavily saturated soils (31). This can especially be an issue in agriculture, where denitrification can reduce fertility and alter microbial metabolism by altering the C/N ratio. At the same time, this service can preserve water quality in agricultural areas due to nitrate runoff if there are riparian buffer wetlands present (31).

Denitrification also plays a role in brownfields, especially brownfield wetlands. Since decomposition of petroleum and hydrocarbons can reduce the oxygen content of the soil, it makes conditions perfect for denitrification. Inorganic N is often a component of urban runoff and is often converted rapidly in brownfield wetlands (32). This conversion exacerbates greenhouse gas emissions that are found in urban areas through the production of N2O, but also can improve water quality of urban watersheds (32).

Lithotropy and Respiration

Rates of respiration are strongly affected by land use changes to brownfield sites because, for many microbes, the concentrations of heavy metals can interfere with essential enzymatic activity (16). Therefore, the microbes that can tolerate these extreme conditions. However, since there may be shortages of carbon substate at a brownfield site, many of these microbes are able to take their reducing equivalents from inorganic sources (17).

Current Research

Dong, X., Y. Huai-Ying, GE De-Yong, and H. Chang-Young. 2007. “Soil Microbial Structure in Diverse Land Use Systems: a Comparative Study Using Biolog, DGGE, and PFLA Analyses”. Pedosphere 18(5):653-663.

Using 3 different molecular methods, the soil microbial community compositions were observed in 3 tea gardens in decreasing age, a secondary growth forest, a “wasteland” consisting of an area populated lightly by grasses. It was found that there is a greater amount of metabolic diversity in the tea garden, followed by the forest, and then the wasteland. Additionally, there was the greatest amount of fungi in the tea garden system according to the fungal PLFA, indicating that land use change encourages increases in soil microbial community structure.


Ding, G-C, Y.M. Piceno, H. Heuer, N. Weinert, A.B. Dohrmann, A. Carrillo, G.L. Andersen, T. Castellanos, C.C. Tebbe, and K. Smalla. 2013. “Changes of Soil Bacterial Diversity as a Consequence of Land Use in a Semi-Arid Ecosystem”. PLOS One 8(3): e59497.

This study looked at the microbial community composition of farm fields that are the conversions of natural shrublands. A 50 year old alfalfa and semi-arid desert sites were compared using DGGE and 16S rRNA gene fragments that were taken from the community DNA. The agricultural soils had less organic matter and phosphates but were more saline. There was an increase in alpha diversity with regards to the agricultural plots, but further analyses of the microbial communities and the physiochemical parameters reveal a decrease in beta diversity.


Hartman, W.H., C.J. Richardson, R. Vilgalys, and G.L. Bruland. 2008. “Environmental and anthropogenic controls over bacterial communities in wetland soils”. PNAS 105(46):17842-17847.

This study looked at factors which dictate wetland soil bacterial abundances and distributions. Samples were taken from North Carolina swamps and bogs across a similar nutrient gradient. Bacterial diversity and community structure were most affected by soil pH, land use, and restoration status. Acidiobacteria and Proteobacteria, in particular, had the most dramatic variation, which could be used for indicators of restoration and trophic status of succession with relation to land use change.

References

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(2) McGrath, D.A., C.K. Smith, H.L. Gholz, and F.A. Oliveira. 2001. “Effects of land-use change on soil nutrient dynamics in Amazonia”. Ecosystems 4:625-645.

(3) Clark, J.J and P.R. Wilcock. 2000. “Effects of land-use change on channel morphology in northeastern Puerto Rico”. Geological Society of America Bulletin 112(12)

(4) Shi, P., X. Ma, Y. Hou, Q. Li, Z. Zhang, S. Qu, C. Chen, T. Cai, and X. Fang. (2013). Effects of Land-Use and Climate Change on Hydrological Processes in the Upstream of Huai River, China. Water Resource Manager 27:1263-1278

(5) Peralta, A.L., J.W. Matthews, A.D. Kent. 2010. “Microbial Community Strtucture and Denitrification in a Wetland Mitigation Bank”. Applied and Environmental Microbiology 76(13):4207-4215

(6) Carlson, T.N. and S. T Arthur. 2000 “Impact of land use-land cover due to urbanization on surface microclimate and hydrology: a satellite perspective”. Global and Planetary Change 25:49-65.

(7) Steenwerth, K.L, L.E Jackson, F.J Calderon, K.M Scow, D.E Rolston. “ Response of microbial comm composition and activity in agricultural and grassland soils after a simulated rainfall”. Soil Biology and Biochemistry 37:2249-2262.

(8) Kimpe, D., C.R., Jean-Louis. 2000. “Urban soil management: a growing concern”. Soil Science 165: 31-40.

(9) Blamey F.P.C, D.G. Edwards, C.J. Asher. 1983 “Effects of aluminum, OH: Al and P:Al molar raiots, and the ionic strength on soybean root elongation in solution culture”. Soil Science 136(4):

(10) Rodriges,J.LM., V.H Pellizari, R.Mueller, K.Baek, E.C. Jesus, F.S. Paula, B. Mirza, G.S. Hamoui, Jr., S.M. Tsai, B. Feigl, J.M. Tiedje, B.J.M.Bohnnan, and K. Nusslein. 2012. “Conversion of Amazon Rainforest to agriculture results in biotic homogenization of soil bacterial communities”. PNAS 110(3).

(11) Ovreas, L and V. Torsvik. 1998. “Microbial diversity and community structure of 2 different agricultural soil communities”. Microbial Ecology 36:303-315.

(12) Jesus, E.D.C., T.L. Marsh, J.M. Tiedje and F.M.D.S Moreira, (2009). “Changes in land use alter the structure of bacterial communities in Western Amazon soils”. The ISME Journal 3:1004-1011

(13) Jangid, K., M.A. Williams,A.J. Franzluebbers. J.S. Sanderlin, J.H. Reeves, M.B. Jenkins, D.M. Endale, D.C. Coleman and W.B. Whitman. 2008. “Relative impacts of land-use, mgmt. intensity, and fertilization upon soil microbial community structure in agricultural systems.” Soil Biology and Biochemistry 40:2843-2853.

(14) Oehl, F., E. Sieverding, K. Ineichen, P. Mader, T. Boller, and Andrews Wiemken. 2003. “Impact of land use intensity on the species diversity of arbuscular mycorrhizae fungi in agroecosystems of central Europe”. Applied and Environmental Microbiology 69(5):2816-2824.

(15) Shi, W., J. Becker, M. Bischoff, R.F. Turco, and A.E. Konopka. (2002). “ Association of microbial community composition and activity with lead, chromium, and hydrocarbon contamination”. Applied and Environmental Microbiology 68(8):3859-3866.

(16) Lorenz, N., T. Hintemann, T. Kramarewa, A. Katayama, T. Yasuta, P, Marschner, and E. Kandeler. 2006. “Response of microbial activity and microbial; community composition in soils to long term arsenic and cadmium exposure”. Soil Biology and Biochemistry 38:1430-1437.

(17) Linton, P.E., L. Shotbolt, and A.D. Thomas. 2007. “Microbial communities in long-term heavy metal contaminatied ombrotropic peats”. Water, Air, & Soil Pollution 186:97-113.

(18) Nordegren, A., E. Baath, and B. Soderstrom. 1983. “:Microfungi and microbial activity along a heavy metal gradient”. Applied and Environmental Microbiology 45(6):1829-1837.

(19) Sandaa,R-A., O. Enger, and V. Torsvik. 1999. “Abundance and diversity of archea in heavy metal contaminated soils”. Applied and Environmental Microbiology 65(8):3293-3297.

(20) Kasai, Y., Y. Takahata, T. Hoaki, and K. Watanabe. 2005. “Physiological and molecular characterization of a microbial community established in unsaturated, petroleum-contaminated soil”. Environmental Microbiology 7(6):806-818..

(21) Deyn, G.B.D., H.Quirk, and R.D. Bardgett. 2010. “Plant species richness, identity, and productivity differentially influence key groups of microbes in grassland soils of contrasting fertility”. Biology Letters.

(22) Kong, C.H., P. Wang, H. Zhao, X.H. Xu, and Y.D. Zhu. 2008. “Impact of allelochemical exuded from allelopathic rice on soil microbial community”. Soil Biology and Biochemistry 40(7):1862-1869.

(23) McLauchlan, K.K., S.E. Hobbie, and W.M. Post. “Conversion from agriculture to grassland builds soil organic matter on decadal timescales”. Ecological Applications 16(1):143-153.

(24) Burger, M., L.E. Jackson. 2003. “Microbial immobilization of ammonium and nitrate in relation to ammonification and nitrification rates in organic and conventional cropping systems”. Soil Biology and Biochemistry 35:29-36.

(25) Dong, X., Y. Huai-Ying, GE De-Yong, and H. Chang-Young. 2007. “Soil Microbial Structure in Diverse Land Use Systems: a Comparative Study Using Biolog, DGGE, and PFLA Analyses”. Pedosphere 18(5):653-663.

(26) Ding, G-C, Y.M. Piceno, H. Heuer, N. Weinert, A.B. Dohrmann, A. Carrillo, G.L. Andersen, T. Castellanos, C.C. Tebbe, and K. Smalla. 2013. “Changes of Soil Bacterial Diversity as a Consequence of Land Use in a Semi-Arid Ecosystem”. PLOS One 8(3): e59497.

(27) Hartman, W.H., C.J. Richardson, R. Vilgalys, and G.L. Bruland. 2008. “Environmental and anthropogenic controls over bacterial communities in wetland soils”. PNAS 105(46):17842-17847.

(28) Munyanziza, E., H.K. Kehri and D.J. Bagyaraj. 1997. "Agricultural intensification, soil biodiversity and agro-ecosystem function in the tropics: the role of mycorrhiza in crops and trees". Applied Soil Ecology 6(1):77-85.

(29) Lauber, C.L., M.S. Strickland, M.A. Bradford, and N. Fierer. 2008. “The influence of soil properties on the structure of bacterial and fungal communities across land-use types”. Soil Biology & Biochemistry 40:2407-2415.

(30) Hartman, W.H., C.J. Richardson, R. Vilgalys, and G.L. Bruland. 2007. “Environmental and anthropogenic controls over bacterial communities in wetland soils”. PNAS 105(46):17842-17847

(31) Cavigelli, M.A. and G.P. Robertson. 2000. “The functional significance of denitrifier community composition in a terrestrial ecosystem”. Ecology 81(5):1402-1414.

(32) Palta, M.M. 2012. “Denitrification in urban brownfield ecosystems”. PhD Dissertation. Rutgers, the State University of New Jersey, New Brunswick, NJ.


Edited by <Jonathan Bressler>, a student of Angela Kent at the University of Illinois at Urbana-Champaign.