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Soil salinity as a driver of microbial community structure and functioning

Rath, Kristin LU (2017)
Abstract (Swedish)
High concentrations of salts in agricultural soils are an environmental problem that has plagued human civilization from its very beginning. Already the earliest civilizations in ancient Mesopotamia struggled with increasing concentrations of salt on irrigated fields. Also in modern times, salinization of soils, particularly of agricultural soils is still a problem restricting agricultural productivity in many areas. Irrigation can make areas suitable for agriculture that would otherwise be too dry to support high crop yields. However, water used for irrigation of fields evaporates and leaves behind dissolved salts, which over time accumulate in the soil to levels that negatively affect growth of crop plants. In order to achieve food... (More)
High concentrations of salts in agricultural soils are an environmental problem that has plagued human civilization from its very beginning. Already the earliest civilizations in ancient Mesopotamia struggled with increasing concentrations of salt on irrigated fields. Also in modern times, salinization of soils, particularly of agricultural soils is still a problem restricting agricultural productivity in many areas. Irrigation can make areas suitable for agriculture that would otherwise be too dry to support high crop yields. However, water used for irrigation of fields evaporates and leaves behind dissolved salts, which over time accumulate in the soil to levels that negatively affect growth of crop plants. In order to achieve food security amidst growing population figures, agricultural productivity will have to be increased. Much of the projected population growth is going to take place in parts of the globe that experience low rainfall year-round or seasonally. Agriculture in these regions is heavily reliant on irrigation with water from groundwater or river sources, and many areas are already suffering from soil salinization. As irrigation agriculture intensifies the area of salt-affected soils will continue to increase.
For plants to be able to grow they need the support of huge numbers of microorganisms that live in soil. This group consists of, as the name suggests, small organisms that are difficult to see without a microscope. Bacteria form one major group of microorganisms. They are tiny single cell organisms that live in the small water-filled space between soil particles. Another major group of soil microorganisms are the fungi. They are well known for the often edible fruiting bodies that some of them produce, but below those fruiting bodies they form vast networks of filaments throughout the soil referred to as hyphae. A single gram of soil can contain billions of bacteria and kilometers of fungal hyphae. Bacteria and fungi are important as decomposers of dead organic material, such as leaf litter and wood. During this process, microorganisms release nutrients bound in plant material that can be taken up by plants. Through their activity as decomposers microorganisms drive the biogeochemical cycling of carbon and nutrients in soil that is necessary to sustain life on earth. While we know much about the effects of soil salinization on plants, we know much less about its impact on microorganisms in soil and the processes carried out by them. Since the extent of salt-affected soils is increasing due to agricultural practices, it is important to understand the impact of salinity on soil microorganisms.
Broadly speaking, effects of environmental changes such as changes in the soil salinity on groups of organisms manifest in two ways. Firstly, they can influence which microorganisms can survive and thrive in the soil, and as a result determine the kind of species one can find at a specific site. This means, environmental change can influence the structure (or composition) of the community. Secondly, environmental conditions can change the microbial activity in the soil, and thus alter the rate at which they carry out all the important processes that microorganisms are responsible for. This means that the functioning of the community changes. These two properties of the community, structure and functioning, are highly interrelated and influence each other.
In this thesis, I studied the various stages in the response of the microbial community to increasing salt concentrations in experimental systems that experienced salinization at different time scales. Firstly I set up very short-term incubations of about one hour with salt added to soil, which covered the initial acute shock without adaptation by the microbial community. When salt is added to a soil, microorganisms will at first experience a shock in response to high salt concentrations. Many of them will die or become inactive, while only some will survive and continue to be active. This can be measured as a reduction in process rates in response to salt exposure. I was interested in how much different functions carried out by soil microorganisms are negatively affected by salinity and what that can tell us about which of these functions may be particularly sensitive to salinization. The processes that I measured included respiration, i.e. the release of CO2 from the soil, which is a measure of the decomposer activity of microorganisms, and several processes involved in N cycling in soils. I also measured the rate at which fungi and bacteria produce new biomass, i.e. their growth rate. All of the processes were strongly inhibited by salt, showing that salinity can impede microbial functioning in soil. The short-term incubations revealed that bacteria are particularly sensitive to acute salt exposure, while fungi could maintain comparatively higher growth rates.
This first set of experiments only covered the immediate aftermath of salt exposure in the community. If given more time, after a short while those microorganisms that could survive the initial shock by salinity will undergo physiological changes that help them deal with the higher salinity. Not all microorganisms, however, have the same potential to adapt to the new salinity, and those species that can tolerate salinity better replace less well-adapted ones. Over time, this change in the species composition towards a community composed of more tolerant species increases the overall community tolerance to salt. To study the changes in microbial community structure and functioning during this adaptive phase, I gave microbial communities from a non-saline soil about one month to adapt to a range of new salinities in second set of experiments. What I was interested in was to see if and how quickly microbial communities can adapt to increasing salinities, and how that increased salt tolerance is reflected in process rates. It turned out that microorganisms could adapt very quickly! Community tolerance increased within a week to a level matched to the soil salinity. At the same time growth rates, which were initially strongly reduced after salt exposure could recover to some degree, but in the end remained lower than process rates in non-saline soil.
How well communities can adapt to salinity is also limited by the pool of species present in the soil before salt addition. In a non-saline soil with no history of salt exposure, such as the one used for experiments 1 and 2 it is unlikely that very many of the species in that soil were able to adapt to high salinity. In places where salinity has had a long time to influence the community and select for salt-tolerant species, it could have resulted in highly adapted communities. The final study system therefore were soils coming from natural salinity gradients, where microbial communities had many years to adapt to the local salinity. Community tolerance strongly increased with salinity, and was accompanied by changes in the bacterial community structure, i.e. we found which bacterial species were salt-tolerant enough to withstand high salinities.
Salinity is not the only pressure that microorganisms in saline soils experience. Areas in which saline soils are common often undergo dry periods during which soils dry out. Drying also inhibits microbial activity in soils and in saline soils the combined impact of salinity and drying could make the effects of the individual factors worse. I tested this by drying soils of different salinity and found that indeed microorganisms were affected more strongly by drying if soils were also saline. Recovery after drying was also slower. After rewetting dried soils to the initial moisture levels, growth and respiration commenced immediately in less saline soils, while in saline soils a lag period of several hours occurred, during which respiration and growth were very low. These findings illustrate that combined environmental stresses can interact and exacerbate their individual effects.
In summary, my research shows that salinity has a strong inhibitory effect on the microbial community. Adaptation to salinity can offset to some degree the loss of functioning provided by the microbial community. This adaptation is accompanied by changes in the structure of the microbial community, i.e. shifts in which species are present in the soil. However, despite communities becoming more tolerant to salinity, some loss of functioning persists. As salt-affected soils are becoming an increasing problem in agriculture, the ability of microorganisms in saline soils to uphold important functions needs to be considered.
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Abstract
Soil salinization is a pressing agricultural problem in many areas of the world, particularly in areas heavily reliant on irrigation agriculture. While the negative effects of salinity on crop plants have been widely studied, its effects on soil microorganisms have received less attention, and the impact of soil salinity on both microbial community structure and functioning is not well understood. Soil microorganisms are important in regulating terrestrial biogeochemical processes and changes in microbial community structure and functioning in response to salinization could have far-reaching consequences for carbon and nutrient cycling.

The main aims of this thesis were to (a) assess and compare the impact of salinity on... (More)
Soil salinization is a pressing agricultural problem in many areas of the world, particularly in areas heavily reliant on irrigation agriculture. While the negative effects of salinity on crop plants have been widely studied, its effects on soil microorganisms have received less attention, and the impact of soil salinity on both microbial community structure and functioning is not well understood. Soil microorganisms are important in regulating terrestrial biogeochemical processes and changes in microbial community structure and functioning in response to salinization could have far-reaching consequences for carbon and nutrient cycling.

The main aims of this thesis were to (a) assess and compare the impact of salinity on different microbial processes in soil, (b) study the ability of soil microbial communities to adapt to increasing salinity and connect increased tolerance to changes in community composition and functioning, and (c) study the combined impact of salinity and another important environmental disturbance, drought. The impact of salinity on soil microorganisms was studied at three different time scales: (i) acute salt exposure, (ii) exposure over one month and (iii) naturally saline soils having experienced high salt concentrations over long time periods.

I found that processes such as growth, respiration and N transformation rates were strongly negatively reduced in response to acute salt exposure. However, increased salt tolerance of the microbial community could be induced quickly, combined with a partial recovery of process rates. A strong relationship between soil salinity and community salt tolerance was also found along natural gradients of salinity. Higher community salt tolerance was reflected in shifts in the composition of the bacterial community. Fungi were less sensitive to salt exposure than bacteria, which manifested in less inhibition of fungal growth both after short-term and long-term exposure to salinity. When salinity was combined with drying of soils, the effects of the individual factors were exacerbated. Increased soil salinity also modified the microbial response to rewetting of died soil.

In summary, soil salinity was found to be an important regulator of both microbial functioning and community composition. While microbial communities have a strong potential to adapt to increasing salt concentrations which can offset to some defree the loss of functioning of the microbial community, process rates are still reduced in saline soils compared to non-saline soils. Thus, as salt-affected soils increase in area, the ability of microorganisms in saline soils to sustain biogeochemical cycles need to be considered.
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Please use this url to cite or link to this publication:
author
supervisor
opponent
  • Prof. Dr. Kandeler, Ellen, University of Hohenheim, Germany
organization
publishing date
type
Thesis
publication status
published
subject
keywords
Soil salinization, Soil Microbiology, soil microbial community, Bacteria, Aerobic, Fungi, Drying-rewetting, Microbial growth, Microbial biomass, Soil respiration, salinity tolerance, Saline soils, Salinity gradient
pages
166 pages
publisher
Lund University, Faculty of Science, Centre for Environmental and Climate Research (CEC)
defense location
Lecture hall “Blå hallen”, Ecology building, Sölvegatan 37, Lund
defense date
2018-01-19 09:30
ISBN
978-91-7753-530-0
978-91-7753-529-4
language
English
LU publication?
yes
id
b3a38a3e-9073-4475-ab6e-efd1f0eb6f42
date added to LUP
2017-12-14 10:22:11
date last changed
2018-01-03 11:08:00
@phdthesis{b3a38a3e-9073-4475-ab6e-efd1f0eb6f42,
  abstract     = {Soil salinization is a pressing agricultural problem in many areas of the world, particularly in areas heavily reliant on irrigation agriculture. While the negative effects of salinity on crop plants have been widely studied, its effects on soil microorganisms have received less attention, and the impact of soil salinity on both microbial community structure and functioning is not well understood. Soil microorganisms are important in regulating terrestrial biogeochemical processes and changes in microbial community structure and functioning in response to salinization could have far-reaching consequences for carbon and nutrient cycling. <br/><br/>The main aims of this thesis were to (a) assess and compare the impact of salinity on different microbial processes in soil, (b) study the ability of soil microbial communities to adapt to increasing salinity and connect increased tolerance to changes in community composition and functioning, and (c) study the combined impact of salinity and another important environmental disturbance, drought. The impact of salinity on soil microorganisms was studied at three different time scales: (i) acute salt exposure, (ii) exposure over one month and (iii) naturally saline soils having experienced high salt concentrations over long time periods. <br/><br/>I found that processes such as growth, respiration and N transformation rates were strongly negatively reduced in response to acute salt exposure. However, increased salt tolerance of the microbial community could be induced quickly, combined with a partial recovery of process rates. A strong relationship between soil salinity and community salt tolerance was also found along natural gradients of salinity. Higher community salt tolerance was reflected in shifts in the composition of the bacterial community. Fungi were less sensitive to salt exposure than bacteria, which manifested in less inhibition of fungal growth both after short-term and long-term exposure to salinity. When salinity was combined with drying of soils, the effects of the individual factors were exacerbated. Increased soil salinity also modified the microbial response to rewetting of died soil.<br/><br/>In summary, soil salinity was found to be an important regulator of both microbial functioning and community composition. While microbial communities have a strong potential to adapt to increasing salt concentrations which can offset to some defree the loss of functioning of the microbial community, process rates are still reduced in saline soils compared to non-saline soils. Thus, as salt-affected soils increase in area, the ability of microorganisms in saline soils to sustain biogeochemical cycles need to be considered.<br/>},
  author       = {Rath, Kristin},
  isbn         = {978-91-7753-530-0 },
  keyword      = {Soil salinization,Soil Microbiology,soil microbial community,Bacteria, Aerobic,Fungi,Drying-rewetting,Microbial growth,Microbial biomass,Soil respiration,salinity tolerance,Saline soils,Salinity gradient},
  language     = {eng},
  pages        = {166},
  publisher    = {Lund University, Faculty of Science, Centre for Environmental and Climate Research (CEC)},
  school       = {Lund University},
  title        = {Soil salinity as a driver of microbial community structure and functioning},
  year         = {2017},
}