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Soil biology for resilient, healthy soil


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Excerpt What is a resilient, healthy soil? A resilient soil is capable of recovering from or adapting to stress, and the health of the living/biological component of the soil is crucial for soil resiliency. Soil health is tightly coupled with the concept of soil quality (table 1), and the terms are frequently used interchangeably. The living component of soil or soil biota represents a small fraction (<0.05% dry weight), but it is essential to many soil functions and overall soil quality. Some of these key functions or services for production agriculture are (1) nutrient provision and cycling, (2) pest and pathogen protection, (3) production of growth factors, (4) water availability, and (5) formation of stable aggregates to reduce the risks of soil erosion and increase water infiltration (table 2). Soil resources and their inherent biological communities are the foundation for agricultural production systems that sustain the human population. The rapidly increasing human population is expanding the demand for food, fiber, feed, and fuel, which is stretching the capacity of the soil resource and contributing to soil degradation. Soil degradation decreases a soil's production capacity to directly supply human demands and decreases a soil's functional capacity to perform numerous critical services, which…
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JAN/FEB 2015—VOL. 70, NO. 1
R. Michael Lehman, Veronica Acosta-Martinez, Jeffrey S. Buyer, Cynthia A. Cambardella, Harold P.
Collins, Thomas F. Ducey, Jonathan J. Halvorson, Virginia L. Jin, Jane M.F. Johnson, Robert J. Kremer,
Jonathan G. Lundgren, Daniel K. Manter, Jude E. Maul, Jeffrey L. Smith, and Diane E. Stott
Soil biology for resilient, healthy soil
R. Michael Lehman is research microbiologist
at the USDA Agricultural Research Service (ARS)
North Central Agricultural Research Laboratory,
Brookings, South Dakota. Veronica Acosta-
Martinez is a research soil scientist at the USDA
ARS Cropping Systems Research Laboratory,
Lubbock, Texas. Jeffrey S. Buyer is a research
chemist at the USDA ARS Sustainable Agricul-
tural Systems Laboratory, Beltsville, Maryland.
Cynthia A. Cambardella is a research soil sci-
entist at the USDA ARS National Laboratory for
Agriculture and the Environment, Ames, Iowa.
Harold P. Collins is a research soil scientist at
the USDA ARS Grassland Soil and Water Re-
search Laboratory, Temple, Texas. Thomas F.
Ducey is a research microbiologist at the USDA
ARS Coastal Plain Soil, Water and Plant Conser-
vation Research Laboratory, Florence, South
Carolina. Jonathan J. Halvorson is a research
soil scientist at the USDA ARS Northern Great
Plains Research Laboratory, Mandan, North Da-
kota. Virginia L. Jin is a research soil scientist at
the USDA ARS Agroecosystem Management Re-
search Unit, Lincoln, Nebraska. Jane M.F. John-
son is a research soil scientist at the USDA ARS
North Central Soil Conservation Research Lab,
Morris, Minnesota. Robert J. Kremer (retired)
is a research microbiologist at the USDA ARS
Cropping Systems and Water Quality Research
Laboratory, Columbia Missouri. Jonathan G.
Lundgren is a research plant physiologist at
the USDA Agricultural Research Service (ARS)
North Central Agricultural Research Laboratory,
Brookings, South Dakota. Daniel K. Manter is
a research soil scientist at the USDA ARS Soil,
Plant, and Nutrient Research Laboratory, Fort
Collins, Colorado. Jude E. Maul is a research
chemist at the USDA ARS Sustainable Agricul-
tural Systems Laboratory, Beltsville, Maryland.
Jeffrey L. Smith (deceased) was a research soil
scientist at the USDA ARS Land Management
and Water Conservation Research Laboratory,
Pullman, Washington. Diane E. Stott is a re-
search soil scientist at the USDA ARS National
Soil Erosion Research Laboratory, West Lafay-
ette, Indiana.
W hat is a resilient, healthy soil?
A resilient soil is capable of
recovering from or adapt-
ing to stress, and the health of the living/
biological component of the soil is cru-
cial for soil resiliency. Soil health is tightly
coupled with the concept of soil quality
(table 1), and the terms are frequently used
interchangeably. The living component of
soil or soil biota represents a small fraction
(<0.05% dry weight), but it is essential to
many soil functions and overall soil qual-
ity. Some of these key functions or services
for production agriculture are (1) nutrient
provision and cycling, (2) pest and patho-
gen protection, (3) production of growth
factors, (4) water availability, and (5) for-
mation of stable aggregates to reduce the
risks of soil erosion and increase water
infiltration (table 2). Soil resources and
their inherent biological communities are
the foundation for agricultural production
systems that sustain the human population.
The rapidly increasing human popula-
tion is expanding the demand for food,
fiber, feed, and fuel, which is stretching the
capacity of the soil resource and contrib-
uting to soil degradation. Soil degradation
decreases a soil’s production capacity
to directly supply human demands and
decreases a soil’s functional capacity to per-
form numerous critical services, which are
valued in trillions of US dollars (Pimental
et al. 1997). The ability to reverse degra-
dation of soil resources and improve soil
services is intimately related to the abil-
ity to promote the biological functioning
or health of the soil. Although this report
primarily considers soil microorganisms,
we fully acknowledge the importance
of higher soil organisms to the mainte-
nance of soil health and provision of soil
services, but leave those phyla to future
discourse. Emerging tools and technolo-
gies have become available to dramatically
advance our understanding of microscopic
soil biota and provide the foundation to
manage soil organisms to enhance primary
productivity, provide multiple ecological
services, rejuvenate soil resilience, and sus-
tain long-term soil resource quality.
The soil has long been perceived to harbor
the greatest microbial diversity among all
ecosystems, and advances in analytical and
computational tools have suggested that
approximately one billion bacterial cells,
grouped into 1,000 to 1,000,000 species,
reside in a single gram of soil (Gans et al.
2005; Schloss and Handelsman 2006). The
rate of discovering and characterizing bac-
terial diversity since 1987 is astounding,
growing from a modest 12 phyla to more
than 70 by 2009 (Pace 2009). However,
many of these phyla contain few, if any,
organisms that can be grown and studied in
the laboratory. Within these new phyla are
bacteria that can fix carbon dioxide (CO2)
via multiple pathways not found in plants
(Thauer 2007) and bacteria that gener-
ate energy from sunlight using alternative
light receptors not previously known (Beja
et al. 2000). Given the recency of these
discoveries, it is not surprising that the
contribution of autotrophic soil bacterial
organisms like these to terrestrial carbon
(C) cycle and C sequestration has not been
determined (Trivedi et al. 2013).
Statement Reference
“Soil quality is the capacity of the soil to function.” Karlen et al. (1997)
Soil health is “the continued capacity of soil to function as a vital Doran et al. (1996)
living system, within ecosystem and land-use boundaries, to sustain
biological productivity, maintain the quality of air and water
environments, and promote plant, animal, and human health.”
Assessment of soil quality is usually accomplished through direct Andrews et al. (2004)
measurement of a suite of soil biological, chemical, and physical
properties and processes that have the greatest sensitivity to
changes in soil function.
Table 1
Soil health is often coupled with the concept of soil quality.
Copyright © 2015 Soil and Water Conservation Society. All rights reserved. 70(1):12A-18A Journal of Soil and Water Conservation
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It is now well-established that all life
can be assigned to one of three domains:
Archaea, Bacteria, and Eucarya (Pace 2009)
(figure 1). Eucarya contains fungi and all
visible (and some microscopic) plant and
animal life. Archaea and Bacteria contain
all of the prokaryotes that are commonly
considered “bacteria” that collectively pos-
sess an enormous diversity of physiologies
and environmental tolerances. In a star-
tling example of the rapidly expanding
knowledge of the microbial world, it was
determined in 2006 that members of the
Archaea domain were actually responsible
for most of the nitrification occurring in
some soils, which had for decades been
thought to be performed strictly by a
very limited number of Bacterial gen-
era (Leininger et al. 2006). Members of a
new phylum of bacteria, Acidobacteria,
whose first representative was discovered
in 1991, were virtually unheard of even 15
years ago and are now suspected to be the
numerically dominant organisms in many
soils. However, due to their resistance to
laboratory culturing, there is insufficient
information to establish their functional
roles. An entirely new class of Fungi
(Archaeorhizomycetes) that closely associ-
ate with plants and are ubiquitous in soils
is just now being described, largely based
on a single cultured member (Rosling et
al. 2011). Other recent discoveries, such
as rampant gene exchange within and
between the three domains by multiple
Table 2
Services provided by soil biota and related processes and benefits (Wall et al. 2004; Falkowski et al. 2008; Kowalchuk et al. 2008;
Pritchard 2011).
Soil functions/properties Processes involved Agronomic services Environmental services
Biogeochemical regulation, Carbon, nitrogen, and phosphorus cycles Provide plant nutrients Mitigate atmospheric gases
nutrient retention and delivery Redox reactions Sequester carbon
Decomposition/humication  Maintain/improvewaterquality
Symbioticandcompensatory Nitrogenxation(bacteria) Provideplantnutrients Maintain/improvewaterquality
associations Nutrient uptake via mycorrhizae (fungi) Enhance water acquisition
Biodegradation/bioremediation of Microbial degradation Reduce pesticide legacy impacts Maintain/improve water quality
wastes, pollutants, and agrochemicals
Pathogen dynamics Host-pathogen interactions Suppress disease Maintain/improve water quality
(regulation and competition)
Soil structure and stability Soil aggregation/porosity Increase aeration Reduce erosion risks
Buildsoilorganicmatter Reducecompaction Mitigateoodanddrought
Improvewaterinltration Sequestercarbon
Increase water holding capacity
Weed dynamics Germination and growth Suppress weed germination, Maintain/improve water quality
growth, and persistence
Figure 1
Tree of Life based rRNA gene sequence comparisons (reprinted with permission
from Pace et al. [2009]).
Copyright © 2015 Soil and Water Conservation Society. All rights reserved. 70(1):12A-18A Journal of Soil and Water Conservation
JAN/FEB 2015—VOL. 70, NO. 1
mechanisms, emphasize the genetic and
functional plasticity of the microscopic
world that exists in soil (Nelson 1999). Gene
exchange has practical implications for
antibiotic resistance (Forsberg et al. 2012)
and also severely complicates attempts to
classify microorganisms, determine their
ecological relationships, and develop useful
models with the predictive power necessary
for management applications.
Advances in analytical and computa-
tional tools have accelerated the rate of
discovery of soil microbial diversity and
enabled renewed efforts to link microbial
community structure to abiotic soil prop-
erties, vegetation, land management, and
climate (figure 2). Because conclusions
often depend on the particular method-
ology selected, the application of multiple
molecular and biochemical assays (table 3)
can be particularly useful. A recent study
exemplifies this multipronged approach
(Maul et al. 2014); these researchers used
quantitative polymerase chain reaction
(qPCR) and terminal restriction fragment
polymorphism (TRFLP) of rRNA genes
and phospholipid fatty acid microbial com-
munity analyses to provide phylum-level
detail of community structure response
to cover crop, mulch, season, and rhizo-
sphere compared to bulk soil. Modern
high throughput DNA sequencing of
soil microorganisms has greatly increased
the ability to characterize the taxonomic
diversity within a particular arable soil
(Acosta-Martinez et al. 2008; Sugiyama
et al. 2010), yet most studies only char-
acterize the dominant taxa (100 to 1,000
species) and provide little insight into the
true genetic diversity and potential pres-
ent in the soil. For example, considering
a typical bacterial genome contains 3,000
to 4,000 genes, the number of microbial
genes present in a single gram of soil may
exceed 1012 genes, or 1,000 terabase pairs
of DNA per gram of soil (Vogel et al.
2009). Assuredly, many great discoveries
and surprises lie ahead.
Soil microbial structures are frequently
used to infer potential functional changes
within the soil microbial community.
Microbial biomass may contribute signifi-
cantly to observed soil functions because
more organisms carrying out a function
may lead to higher rates of that function.
Although there is an emerging under-
standing of the redundancy that exists
within the soil microbial community gene
pool, it is still unclear if there are (1) a
small number of species that dominate the
transcriptome (collection of all mRNA
transcripts), (2) rare groups that dominate
intermittently based on environmental
conditions, or (3) microbial consortia that
express genes in a coordinated fashion
resulting in observed microbial com-
munity functionality. Linking microbial
composition and biomass (e.g., who and
how many) to analysis of soil microbial
gene expression will be key to unravel-
ing the regulation of soil functions that are
desirable in agroecosystems.
It has often been assumed that changes
in the phylogenetic community structure
lead to changes in soil functionality as a
result of differential niche specializations
that have evolved among phyla. For exam-
ple, certain functions can be associated with
particular genera or species, (e.g., nitrogen
[N] fixation). As more genomic informa-
tion is collected within each phylogenetic
clade, however, it is becoming clear that
functional redundancy is most likely the
norm among widely divergent microbial
groups (Allison and Martiny 2008; Ollivier
et al. 2012). Although individuals within a
species or genera may all contain genes to
carry out a specific function, it is rare that a
specific function is exclusively maintained
within only a single genera or species. This
Figure 2
Selected factors affecting soil functions and the provision of ecosystem services. The arrow represents interactions between fac-
tors and within each factor.
Copyright © 2015 Soil and Water Conservation Society. All rights reserved. 70(1):12A-18A Journal of Soil and Water Conservation
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Method Notes Benetstosoilproduction Advantages Disadvantages
(Automated)ribosomalintergenic DNAproles/patterns Diversityhasbeenused Highthroughput,costeffec- Subjecttooverestimation
spacer analysis ([A]RISA) generated for each to assess soil health. tive, low technical demand. of species richness.
AmpliedribosomalDNA bacterialcommunity. Microbialcommunity Costeffective,low Mosteffectivetosubtype
restriction analysis (ARDRA) Data is generated as responses to changing technical demand, no individual species due to
polymerase chain soil conditions can also specialized equipment generating multiple
reaction amplicons or serve as a determinant necessary. bands per species.
Length-heterogeneity polymerase fragments separated of soil health. High High throughput, highly Limited database support.
chain reaction (LH-PCR) by size (e.g., T-RFLP) throughput, low cost, reproducible, cost effective.
(Denaturing/temperature) gradient or sequence (e.g., DGGE). and reproducible nature Fragments can be extracted Variability between gels/
gelelectrophoreses([D/T]GGE) Somemethodsallow ofseveralngerprinting andsequenced. experimentsmakesgel
fordownstream methodsmakethem  togelcomparisonsdifcult.
Randomampliedpolymorphic processing(e.g.,DGGE) suitableforlong-term Rapid,highthroughput, Randomnatureofampli-
DNA(RAPD) formethodssuchas monitoringofsoils.Can costeffective,low cationcouldbeaffected
DNA sequencing. be used for monitoring technical demand. by DNA quality resulting
Generally good for large areas and could be in low reproducibility.
Single-strand conformation comparing community considered as potential Fragments can be extracted Reannealing of DNA strands
polymorphism (SSCP) structure, possibly standardized soil tests. and sequenced. Can identify can increase number
diversity. Require new mutations. of bands. Heteroduplex
specialized software DNA can be formed.
Terminal-restriction fragment for post-run analysis Rapid, high throughput, Fragments cannot be
length polymorphism (T-RFLP) and comparison. cost effective, method sequenced, distinct
can be applied to microbial groups may share
multiplegenetargets. prole.
Sequence-based methods
Clone libraries Provides DNA (e.g., Provide insight into the Low degree of specialized Time consuming, lower
pyrosequence) or RNA following soil microbial equipment required. throughput than
(e.g.,metatranscriptomics) characteristics: pyrosequencing methods,
sequence either directly abundances (e.g., cloning biases.
Small subunit (SSU) rDNA/rRNA or based on qPCR); diversity (e.g., Low cost per base pair rDNA generally fails to
pyrosequencing hybridization (e.g., 16S rRNA); and of sequence. SSU rRNA distinguish between
microarray). Can allow potential microbial universally found, and microbes actively growing,
for microbial activity (e.g., contains conserved dead, or in stasis. High
identicationdownto metatranscriptomics, regionsthatallowfor equipmentcosts.Bias
genus and species levels. qRT-PCR). Information phylogenetic discrimination. with DNA/RNA extraction
Provide excellent can be measured both methods and SSU
estimatesofmicrobial temporallyand rDNA/rRNAamplication.
Metagenomics activity, biomass, and spatially, allowing for Provides insight into meta- Costly to achieve high
diversity. If not correlations with bolic pathways of entire coverage rates of microbial
contracted to an outside environmental microbial community. Can community. Does not indicate
party, these techniques conditions. Depending result in comp lete which spec ies are active or
come with considerable on the method, data sequencing of previously in stasis. Data analysis is
start-upcostsfor generatedcanbevery unidentiedanduncultured complex,computer
equipmentandreagents, specic(e.g.,qPCR)or microbialspecies.No intensive,andtime
though their high broad in nature. In- reliance on known sequences. consuming.
Metatranscriptomics throughput, big data, depth analysis of soil Provides information on gene In bacteria, rRNA accounts
naturegenerallytendsto microbialsystemsnot expressionprolesof for95%oftotalRNA,
reduce costs on a per provided by other bacterial community at bacterial rRNA removal
basepairrate.Fora techniquesandcan timeofsampling, difcultandintroduces 
number of these help identify management indicating potential responses biases. Based on assump-
methods,bioinformatics practicesthatarebenecial toenvironmentalcues.As tionsthatRNAwillbe
can be a bottleneck. or deleterious to microbial with metagenomics, sequence translated into protein
communities. can be unknown beforehand. and subsequently activity.
Table 3
Techniques for soil microbial ecology analysis (Hill et al. 2000; Hirsch et al. 2010; Rincon-Florez et al. 2013).
Table 3 Continued
Copyright © 2015 Soil and Water Conservation Society. All rights reserved. 70(1):12A-18A Journal of Soil and Water Conservation
JAN/FEB 2015—VOL. 70, NO. 1
is, in part, due to (1) relatively quick gen-
eration times, which allow for adaptation
to environmental variation; (2) ability for
many microbes to carry out conjugation
and the passage of plasmid-borne genes
and elements among individuals; and (3)
genetic competence, which enables hori-
zontal gene transfer across different genera
and facilitates uptake and genomic inte-
gration of exogenous DNA. As a result,
the distribution of many functional traits
across unrelated taxa creates questions as
to the accuracy of using microbial com-
munity phylogenetic (structural) data to
infer functional changes within a particu-
lar community. But, true in situ functional
measurements of specific soil microbial
activities are quite elusive, as the act of
making a measurement or collecting a
sample alters microbial activities.
Despite these challenges, the relation-
ship between soil microbial community
structure and function and whether they
respond in unison to their local envi-
ronment determines the best approaches
to gauge management effects on the
collective function of soil microbial com-
munities. Ecological hypotheses regarding
the biogeography of soil microorgan-
isms and the potential for endemic soil
microbial populations have been used to
examine community structure-function
relationships and evaluate functional
redundancy. A combination of high
throughput DNA sequencing and enzyme
activity were applied to soil fungal com-
munities in a study that spanned local
and continental scales (Talbot et al. 2014).
These researchers found that some fungi
were endemic (unique) to certain locales,
while overall community function was
similar across all the sites. Wholesale
quantification of soil microbial allele
frequency (gDNA) and transcript abun-
dance (mRNA)—an inventory of genetic
potential and activity generally known as
“metagenomics”—has also been used to
address this same question. In contrast to
the findings of the previous study, these
researchers found strong correspondence
between functional and structural diversity
in soil microbial communities from glob-
ally distributed sites (Fierer et al. 2012). In
a separate metagenomic study of prairie
soil bacterial communities, a single phy-
lum, Verrucomicrobia, was responsible for
much of the biogeographical variation
observed and provided evidence in oppo-
sition to functional redundancy (Fierer et
al. 2013). The extent of microbial species
endemism and functional redundancy are
central to measurement of soil health and
resilience, particularly in relation to biodi-
versity (Griffiths and Philippot 2013).
The ability to sequence environmen-
tal DNA to the depth currently available
has changed the questions that can be
posed when exploring the soil microbial
ecosystem. Soil nuclear metagenomes are
being explored as snapshots of varied envi-
ronments, but there are few examples of
replicated sites with a priori agricultural
Table 3 continued
Method Notes Benetstosoilproduction Advantages Disadvantages
Sequence-based methods (continued)
Microarrays Canbeusedforanalysisof Nonspecichybridization,
DNA or RNA. A large time consuming array
amount of information construction requires
placed on a single array. expensive equipment, target
determined a priori.
quantitativepolymerasechain Rapid,reproducible,cost Primerbias,uorescent
reaction (qPCR) (DNA)/ reverse effective, high sensitivity. probe options limit analysis
transcriptase polymerase chain Primer sets can be of to a few targets per assay,
reaction(qRT-PCR)(RNA) narroworbroadspecicity, targetsbasedonlyon
each microbial gene can known sequences.
serve as a target for study.
Other methods
Culturing Providebiomarker(e.g., Metabolicallyactive Isolatedmicrobesare Lowthroughput,difcult
PLFA, FISH) or soil microbes (except available for additional or impossible to grow
biochemical data (e.g., PLFA). Can study analysis and characterization. many soil microbes.
Communitylevelphysiological community-level specicorganismal Moderatethroughput; Lowerdiscriminatorypower;
proling physiologicalprole interactions(e.g.,FISH) insightsintoheterotrophic oftenbiastowardfaster
[CLPP]) of select microbial and preference for substrate usage; new, improved growing microbes,
species or whole carbon substrates (e.g., platforms are available particularly Biolog.
Fluorescent in situ communities. Not high CLPP). PLFA have data Multiple probes can be Traditional methodology is
hybridization (FISH) throughput in nature, and foundation for used simultaneously. not quantitative. Some
some require comparative studies Highly sensitive, detect probes may not effectively
sophisticated equipment between ecosystems. single cell in complex penetrate certain cells.
for analysis of environments.
Phospholipid fatty acid (PLFA) samples (e.g., FISH). Biomass, community Coarse resolution; lower
structure. throughput, improved with
microplate format.
Copyright © 2015 Soil and Water Conservation Society. All rights reserved. 70(1):12A-18A Journal of Soil and Water Conservation
JAN/FEB 2015—VOL. 70, NO. 1
management treatments being tested. This
limits evaluations of the environmental or
agricultural management drivers respon-
sible for functional changes within with the
soil microbial community. In a recent break-
through, microarray approaches were used
to measure functional gene abundances in
replicated field plot soils under high input
(i.e., conventional) versus low input (con-
servation) agricultural management (Xue et
al. 2013). These authors made two notable
findings: (a) the abundance of functional
genes for N transformations (denitrification
and ammonification) was closely linked
with independent measures of soil N pools
and fluxes; and (b) functional gene diversity
was significantly higher in the low input
production system compared to the high
input production system.
Ultimately, soil health and resilience will
rely on maintaining functionally diverse,
robust soil biological communities that
support high levels of critical services, sim-
ply by carrying out their life-sustaining
processes. Experimentally, soil biodiver-
sity has been strongly associated with
key ecosystem functions such as decom-
position and nutrient cycling (Wagg et
al. 2014). Some agricultural management
practices can have negative effects on soil
health, while other practices are more
conducive to soil biological health (figure
3). Much of the data that supports exist-
ing soil health assessments of agricultural
management practices is based on bulk
soil measures like biomass, respiration, or
enzyme activity. In a relatively few cases,
specialized organisms such as the obligate
biotropic arbuscular mycorrhizal fungi
(AMF) have been used to demonstrate
positive effects of conservation agricul-
tural practices like cover cropping on soil
health (Lehman et al. 2012). However,
limited knowledge of AMF ecology, fluid
taxonomic assignments, and inadequate
analysis tools currently restrict application
of this specific approach in numerous field
applications. Similarly, there is inadequate
knowledge concerning the soil microbial
consortia responsible for weed (Kremer
and Li 2003) and pathogen (Mendes et
al. 2013) suppressive soils, or the ecology
of plant growth promoting rhizobacteria
(Zahir and Frankenberger 2004) to take
advantage of these biological services.
The challenge at hand is to use the
emerging basic knowledge of soil micro-
bial diversity and modern analytical
tools in the testing of relevant ecological
hypotheses (e.g., endemism and functional
redundancy) under differing agricul-
tural management practices. Since soil
type, climate, and vegetation, and local
management practices are known to influ-
ence soil microbial communities and vary
regionally, research must be performed at
regionally distributed sites by multidis-
ciplinary teams. The known seasonality
effects on soil microbiological dynamics
must be accounted for with temporally
dense sampling schemes. The outcome of
this science will serve as the basis to answer
the following questions that are central to
promoting soil health and resiliency:
1. What are the most useful measures of
soil health?
2. How is soil health linked to manage-
ment decisions, including the use of
biological amendments?
3. What benefits does soil health have for
the individual producer/rancher?
Answering these questions in a scien-
tifically defensible manner will promote
agricultural practices that take full advan-
tage of the services provided by soil biota
while maintaining or improving soil health
and resilience.
Acosta-Martinez, V., S.E. Dowd, Y. Sun, and V.G. Allen.
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Copyright © 2015 Soil and Water Conservation Society. All rights reserved. 70(1):12A-18A Journal of Soil and Water Conservation
... To address the limitations of static measurements, changes in microbial indicators within the same field provide more insight in the soil health status. This is related to the fact that soil microorganisms respond sensitively to disturbances in their surroundings, and may be more susceptible to these disturbances when soil health deteriorates (Lehman et al., 2015). This suggests that the response of microorganisms subjected to disturbances have the potential to act as bio-indicators for soil health (Allison and Martiny, 2008;Kibblewhite et al., 2008;Cardoso et al., 2013;Fierer et al., 2021). ...
... Fungi tend to be more drought-tolerant than bacteria, as the hyphal network covers a larger area and can transport water and nutrients (Sun et al., 2017;de Vries et al., 2018). However, the sensitivity towards drying-rewetting disturbances can be linked to soil health as it has been shown that land use could determine the microbial resiliene to drying-rewetting (Lehman et al., 2015;Brangarí et al., 2022). We therefore assume that within healthier soils, the soil microbiome is more resilient against drying-rewetting disturbances in controlled incubator experiments. ...
... Conventional practices cause loss of the diversity, microbial population and activity of soil fauna thereby adversely affecting soil health and resilience of agroecosystems (Choudhary et al., 2018a,b;Singh et al., 2018). Lehman et al. (2015) highlighted the role of soil biology in soil health and illustrated how biological properties and processes contribute to sustainability of agriculture and ecosystem services. ...
... Enzyme activities in soil such as DHA, FDA and hydrolases (e.g., urease, protease, phosphatase and β-glucosidase) and amylase, arylsulphatase, cellulase and chitinase, are important indicators of soil health (Bera et al., 2018;Das and Varma, 2011;Sharma et al., 2021). The enzyme activities are frequently more sensitive to land management and environmental stress than physical and chemical indicators (Choudhary et al., 2018a,b;Lehman et al., 2015). ...
... The biological properties of a soil can be assessed using indicators such as organic matter content, microbial biomass, soil respiration, and enzymatic activity (Allen et al., 2011). The microbiota of agricultural soils is composed of complex microbial communities, and recent developments in metagenomic analyses have made it possible to study more precisely the behavior of these communities when exposed to various farming practices (Lehman et al., 2015;Wall et al., 2019). Assessing the richness and composition of bacterial and eukaryotic communities could enable the selection of appropriate biological indicators of agricultural soil health (Lehman et al., 2015;Sahu et al., 2018;Trivedi et al., 2016). ...
... The microbiota of agricultural soils is composed of complex microbial communities, and recent developments in metagenomic analyses have made it possible to study more precisely the behavior of these communities when exposed to various farming practices (Lehman et al., 2015;Wall et al., 2019). Assessing the richness and composition of bacterial and eukaryotic communities could enable the selection of appropriate biological indicators of agricultural soil health (Lehman et al., 2015;Sahu et al., 2018;Trivedi et al., 2016). Deep plowing of agricultural soils is a weed management practice that mechanically alters the soil structure, causing surface erosion and deep compaction (Baumhardt et al., 2015). ...
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Intensive agriculture based on repeatedly plowing a monoculture is known to degrade the structural, chemical, and biological properties of soils. Conservation agriculture is gaining popularity worldwide with practices including reduced tillage, increased plant diversity, and implementation cover crops. The aim of this study was to assess the impact of crop rotation and cover crops on soil microbial communities. The hypothesis was that enhanced plant diversity would boost the diversity of the soil microbiome. Two rotation were tested by adding a cereal (corn [Zea mays L.]–soybean [Glycine max (L.) Merr.] and corn–soybean–wheat [Triticum aestivum L.]), as well as the implementation of cover crops. The enhanced plant diversity had no impact on total molecular biomass. The bacteria/fungi ratio varied across the plots but was not clearly linked to the enhanced plant diversity. Bacterial richness was not influenced by the treatments, whereas eukaryotic richness decreased in the presence of cover crops in one of the sites. Microbial composition was the most sensitive indicator to enhanced plant diversity. Differential relative abundance (log2 fold changes) identified proteobacterial amplicon sequence variants (ASVs) specifically related to each crop rotation system and to the presence of cover crops. There was more ASV of Actinobacteria associated with the three‐crop rotation system and less ASV of Acidobacteria associated with the cover crops system compared to the two‐ and three‐crop rotation systems, respectively. As for eukaryotes, the number of ASVs belonging to Ascomycota and Cercozoa phyla and associated with the three‐crop rotation system is less important than for the two‐crop rotation system. This study shows that conservation agricultural practices can influence soil microbial communities. The variations in some ASVs could have functional implications on organic matter decomposition or plant growth and in terms of soil ecosystem services and field crop sustainability. Crop rotation and cover crops can both influence bacterial composition. Microbial composition is more sensitive to plant diversity than molecular biomass and microbial richness. Eucaryotic richness and composition are influenced negatively by plant diversity enhancement.
... While soil health is associated with sustainable agriculture [8,9], it degrades soil in the long run due to supplying food for the ever-increasing human population [10,11], robbing the soil of its production capacity and food-generating ability [11,12]. Agricultural practices deprive soil properties [2,13] have been reported in Uruguay after an agricultural production period between 2012 and 2014 [14], in Iran after forestland conversion to tea plantation [15], and in Italy where food self-sufficiency plummeted to less than 80 % [12]. ...
... While soil health is associated with sustainable agriculture [8,9], it degrades soil in the long run due to supplying food for the ever-increasing human population [10,11], robbing the soil of its production capacity and food-generating ability [11,12]. Agricultural practices deprive soil properties [2,13] have been reported in Uruguay after an agricultural production period between 2012 and 2014 [14], in Iran after forestland conversion to tea plantation [15], and in Italy where food self-sufficiency plummeted to less than 80 % [12]. ...
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Soil is paramount to sustaining living in biomass production, water quality control, climatic mitigation, and biodiversity endurance. Closely associated with sustainable agriculture, it degrades soil in the long run, robbing the soil of its production capacity and food-generating ability. In Probolinggo, a regency in Indonesia, intensifying the use of chemical fertilizers and pesticides yet a declining trend in yield production was discovered. This research analyzed the acid, nitrogen, organic carbon, and nutrients focusing on phosphor, potassium, iron, and manganese contents. Organic carbon/nitrogen ratio, soil organic compound rate, and cation exchange capacity were also discussed in order to illustrate the correlations among chemical substances and their roles in soil and plant maintenance. While such a study has yet to be performed in Probolinggo, the results should show the degree of land deterioration and future attempts at damage control and correction open to facilitate. Employing a simple random method, soil and plant samples were collected from 18 villages in six districts and their chemical contents were compared to the standard set in Government Regulations No 150/2000. The results showed low N-total, P-Bray, P-Olsen, K, C-Organic, and C/N ratio availabilities at 0.18, 13.88, 14.41, 0.37, 1.36, and 7.38 respectively, contrasted to high rates on pH (5.94), Fe (153.46 mg kg–1) and Mn (37.96 mg kg–1). Biomass production is conclusively imperative to fix the land composition and meet the plant nutrient requirements through an organic approach; fertilizers from digester biogas are therefore recommended. This action requires field agricultural advisors to raise awareness of sustainable agriculture.
... Microorganisms are responsible for driving es-sential ecosystem processes such as nutrient cycling, OM decomposition, plant nutrient uptake, and maintenance of soil structure (Dangi et al., 2020;Pérez-Guzmán et al., 2020;Dangi et al., 2013;Dangi et al., 2012) and are particularly sensitive to changes in soil quality due to wildfire or prescribed fire disturbances (Barreiro and Díaz-Raviña, 2021). Soil health and quality depend on maintaining diverse and vigorous biological communities that are responsible for these processes (Lehman et al., 2015). Fires alter SMC activity and composition directly through heat-induced microbial mortality (DeBano et al., 1998;Hart et al., 2005), and the post-fire soil recovery is determined to great extent by its impact on soil microorganisms (Barreiro and Díaz-Raviña, 2021). ...
Field fires can modify soil nutrient cycling and alter soil microbial communities (SMC), although the latter is not well understood. In the southern region of Puerto Rico, field fires have become a significant problem during the dry season. To mimic the effects of a field fire, we performed prescribed fires on a hillside at the Juana Díaz Agricultural Experiment substation in October 2015 and March 2017. A complete randomized block design was established in Yauco soil (Typic calciustolls) that included the following treatments: negative control (unburned), positive control (burned plots, no remediation), mulching treatment (burned plots remediated with Leucaena spp. mulch), and surfactant treatment (burned plots remediated with a surfactant). In the first burning (2015), soil samples were collected before burning and at 30, 180, and 420 days after burning (DAB). In the second burning (2017), soil samples were collected at 30, 90, and 270 DAb. soil physicochemical properties and microbial community structure were assessed using phospholipid fatty acid (PLFA) analysis. Overall, burning increased soil exchangeable Ca2+ (except after 30 DAB in the second burning) and decreased exchangeable K+ when compared to unburned soils. compared to unburned plots, total fungal PLFA was significantly lower in burned plots with or without mulch and surfactant treatments, and total bacterial PLFA did not differ between burned and unburned plots after 30 days. Total microbial biomass was significantly (P<0.05) higher in mulch and surfactant treated burned soil compared to unburned and burned plots without treatment after 90 DAB (2017) and 420 (2015) DAB. The use of mulch and surfactant treatments in prescribed burning fields increased microbial communities 90 DAB. This study emphasizes short-term changes in microbial communities and suggests they are highly resilient to disturbances after prescribed fires.
... This is because they are the major drivers of SOM mineralization (Duchicela et al., 2012) This SOM mineralization lead to higher rates of soil respiration (Mbuthia et al., 2015). Microbial communities are also critical for plant health, as they control soil-borne pathogens (Senechkin et al., 2010;van Bruggen et al., 2015), and are also involved in soil responses after disturbance (Lehman et al., 2015). Diverse soil microbial communities may also contribute to alleviating soil salinity and other stressful conditions (Kumar et al., 2020). ...
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Aim of study: Intensive agriculture impacts physical, chemical, and biological characteristics of soil; therefore, the addition of organic matter (OM) to soil can have significant implications for crop production. This study investigated the impact of three crop management systems on tomato production and soil microbial communities in intensive greenhouse farming. Area of study: Province of Almería (Spain). Material and methods: The three crop management systems included: (1) conventional management, using synthetic chemical fertilizers without OM application (CM); (2) conventional management, using synthetic chemical fertilizers with at least one OM application in the last three years (CMOM); and (3) fully organic management, featuring yearly OM applications and no use of synthetic chemical fertilizers (ORG). Main results: Compared to CM soils, OM addition in CMOM and ORG led to higher soil NO3- and NH4+ content, which in turn increased nitrogen (N) availability, leading to an increase in soil respiration. The addition of OM also altered the composition of prokaryotic and fungal soil communities. Besides, the addition of OM reduced the presence and abundance of potential fungal pathogenic organisms, like Sclerotinia sp. and Plectosphaerella cucumerina. OM addition to conventionally managed greenhouses (CMOM) led to higher crop yields compared to CM greenhouses, resulting in an overall increase of 880 g m-2. Production under fully organic management (ORG) was lowest, possibly due to the nutrient and pest management practices used. Research highlights: Our data show the importance of organic matter management in shaping microbial communities in intensive greenhouse systems, which can be a key factor in developing a more sustainable agriculture to feed a growing human population.
Soils are dynamic and subject to numerous degradative processes (e.g., erosion, compaction, salinization, acidification). Most of all, climatic fluctuations including frequent droughts, floods, and heat waves, intense rainstorms, and other extremes are the leading stressors of soil (Smith et al. 2022). No soil is free of degradation unless properly managed or adjusted to navigate the persistent degradative processes (Hirsch et al. 2017). The ability of a soil to continue provisioning all vital ecosystem services in spite of the degradative processes is of paramount importance to ecosystem health (Ludwig et al. 2018). This inherent characteristic of a soil is termed as soil resilience.
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Mycorrhizal fungus diversity is an ecosystem health indicator, and thus, the appreciation of the aboveground as well as the belowground biota, such as fungi associated with natural and managed ecosystems, is essential to provide sustainable products and suggestions to farmers. Less is known about the totally arbuscular mycorrhizal fungi (AMF) and fungal endophytes useful to agroecology, which are environment friendly microbial biofertilizers to mitigate the complications of conventional farming. Specific AMF are found in most covers; grassy ecosystems are increasingly investigated through their exclusive fungal species that improve sustainable cultivation. Different grazed pastures, forages, and their diversity are important objects of study either in economic or ecological scope. Based on recent reports, the occurrence of AMF in grasslands and pastures is significant, supporting more diverse AMF than native forests. Therefore, we show current information on these topics. We conducted a Web of Science search of published articles on AMF, pastures, and grasslands and analyzed them. The results confirmed the important role of pH as the driver of AMF diversity distribution between the grassy ecosystems from Argentina and Brazil. In grasslands, the main family represented was Glomeraceae, while pastures maintain predominantly Acaulosporaceae. Brazilian grasslands and pastures presented four times the AMF richness of those from Argentina.
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Healthy soils provide the foundation for sustainable agriculture. However, soil health degradation has been a significant challenge for agricultural sustainability and environmental quality in water-limited environments, such as arid and semi-arid regions. The soil in these regions is often characterized by low soil organic matter (SOM), poor fertility, and low overall productivity, thus limiting the ability to build SOM. Soil health assessment frameworks developed for more productive, humid, temperate environments typically emphasize building SOM as a key to soil health and have identified the best management practices that are often difficult to implement in regions with water limitations. This study reviewed existing soil health assessment frameworks to assess their potential relevance for water-limited environments and highlights the need to develop a framework that links soil health with key ecosystem functions in dry climates. It also discusses management strategies for improving soil health, including tillage and residue management, organic amendments, and cropping system diversification and intensification. The assessment of indicators sensitive to water management practices could provide valuable information in designing soil health assessment frameworks for arid and semi-arid regions. The responses of soil health indicators are generally greater when multiple complementary soil health management practices are integrated, leading to the resilience and sustainability of agriculture in water-limited environments.
Agriculture is actually facing reduced production, increasing costs, and increasing resistance of plant pathogens and other pests. The extensive usage of agrochemicals, monoculture, and soil pollution have deteriorated soil health. Poor management practices have altered the soil biology, deteriorated the soil structure, and reduced the soil organic matter content, calling for more sustainable management such as the use of microorganisms for rejuvenating degraded soils. Here we review the improvement of soil health with microorganisms with focus on carbon sequestration, nutrient cycling, degradation of contaminants, reduction of plant pathogens, and reduced usage of fertilizers.
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Significance Microbes control vital ecosystem processes like carbon storage and nutrient recycling. Although megadiversity is a hallmark of microbial communities in nature, we still do not know how microbial diversity determines ecosystem function. We addressed this issue by isolating different geographic and local processes hypothesized to shape fungal community composition and activity in pine forests across the continental United States. Although soil enzyme activity varied across soils according to resource availability, enzyme activity was similar across different fungal communities. These observations indicate that much of fungal diversity plays an equal role in soil biogeochemical cycles. However, soil fungal communities vary dramatically in space, indicating that individual species are endemic to bioregions within the North American continent.
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Significance Biological diversity is the foundation for the maintenance of ecosystems. Consequently it is thought that anthropogenic activities that reduce the diversity in ecosystems threaten ecosystem performance. A large proportion of the biodiversity within terrestrial ecosystems is hidden below ground in soils, and the impact of altering its diversity and composition on the performance of ecosystems is still poorly understood. Using a novel experimental system to alter levels of soil biodiversity and community composition, we found that reductions in the abundance and presence of soil organisms results in the decline of multiple ecosystem functions, including plant diversity and nutrient cycling and retention. This suggests that below-ground biodiversity is a key resource for maintaining the functioning of ecosystems.
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Prairie Redux Tallgrass prairie is extinct across much of its former range in the midwestern United States, but relicts preserved in cemeteries and nature reserves allow functional comparison of former grassland soils with modern agricultural soils. Fierer et al. (p. 621 ; see the Perspective by Scholes and Scholes ) took matched soil samples from sites representing the gamut of climate conditions and modeled the combination of genomic analysis and environmental data to resurrect the historical prairie soil communities, identifying the nutrient-scavenging Verrucomicrobia as keystone bacteria in functioning prairie.
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Soil microbial communities play an important role in plant health and soil quality. Researchers have developed a wide range of methods for studying the structure, diversity, and activity of microbes to better understand soil biology and plant-microbe interactions. Functional microbiological analyses of the rhizosphere have given new insights into the role of microbial communities in plant nutrition and plant protection against diseases. In this review, we present the most commonly used traditional as well as new culture-independent molecular methods to assess the diversity and function of soil microbial communities. Furthermore, we discuss advantages and disadvantages of these techniques and provide a perspective on emerging technologies for soil microbial community profiling.
Understanding microbial responses to crop rotation and legacy of cropping history can assist in determining how land use management impacts microbially mediated soil processes. In the literature, one finds mixed results when attempting to determine the major environmental and biological controls on soil microbial structure and functionality. The objectives of this research were to: (1) Qualitatively and quantitatively measure seasonal and antecedent soil management effects on the soil microbial community structure in the rhizosphere of a subsequent tomato crop (Solanum lycopersicum) and (2) Determine phylum scale differences between the rhizosphere and bulk soil microbial community as influenced by the antecedent hairy vetch (Vicia villosa), cereal rye (Secale cereale), or black plastic mulch treatments. In this report, we use terminal restriction fragment length polymorphisms in the 16s rDNA gene to characterize changes in microbial community structure in soil samples from a field replicated tomato production system experiment at USDA-ARS Beltsville Agricultural Research Center, Beltsville, MD, USA. We found season of the year had the strongest influence on the soil microbial community structure of some of the major microbial phyla. Although we monitored just a few of the major microbial phyla (four Eubacteria and Archaea), we found that the effects of the tomato plant on the structural composition of these phyla in the rhizosphere differed dependent on the antecedent cover crop. Increased understanding of how agricultural factors influence the soil microbial community structure under field conditions is critical information for farmers and land managers to make decisions when targeting soil ecosystem services that are microbially driven.
There is an urgent need for novel agronomic improvements capable of boosting crop yields while alleviating environmental impacts. One such approach is the use of optimized crop rotations. However, a set of measurements that can serve as guiding principles for the design of crop rotations is lacking. Crop rotations take advantage of niche complementarity, enabling the optimization of nutrient use and the reduction of pests and specialist pathogen loads. However, despite the recognized importance of plant-soil microbial interactions and feedbacks for crop yield and soil health, this is ignored in the selection and management of crops for rotation systems. We review the literature and propose criteria for the design of crop rotations focusing on the roles of soil biota and feedback on crop productivity and soil health. We consider that identifying specific key organisms or consortia capable of influencing plant productivity is more important as a predictor of soil health and crop productivity than assessing the overall soil microbial diversity per se. As such, we propose that setting up soil-feedback studies and applying genetic sequencing tools towards the development of soil biotic community databases has a strong potential to enable the establishment of improved soil health indicators for optimised crop rotations.
Soil organic carbon performs a number of functions in ecosystems and it is clear that microbial communities play important roles in land-atmosphere carbon (C) exchange and soil C storage. In this review, we discuss microbial modulators of soil C storage, 'omics'-based approaches to characterize microbial system interactions impacting terrestrial C sequestration, and how data related to microbial composition and activities can be incorporated into mechanistic and predictive models. We argue that although making direct linkage of genomes to global phenomena is a significant challenge, many connections at intermediate scales are viable with integrated application of new systems biology approaches and powerful analytical and modelling techniques. This integration could enhance our capability to develop and evaluate microbial strategies for capturing and sequestering atmospheric CO2.
Intensive agricultural practices, such as tillage, monocropping, seasonal fallow periods, and inorganic nutrient application have been shown to reduce arbuscular mycorrrhizal fungi (AMF) populations and thus may reduce benefits frequently provided to crops by AMF, such as nutrient acquisition, disease resistance and drought tolerance. We have evaluated the ability of different cover crops to elevate the native mycorrhizal inoculum potential of soils under soil–climatic conditions typical of the upper Midwest U.S. production agricultural region. We measured the number of soil AMF propagules at three sites in the late fall following cover crops that were seeded into summer-harvested small grains within a no-till rotation. At all three sites, soil AMF propagule numbers were generally low (≤1 propagule g−1). Fall cover crops significantly increased the mycorrhizal inoculum potential of the soils. Forage oats (Avena sativa (L.) Hausskn.), by itself or in mixtures, was most effective at both sites where it was planted. At the third site, a cover crop mixture doubled the inoculum potential of these soils. The effect of cover crop treatments on AMF propagules was corroborated at one site over two seasons by measuring AMF biomass with the neutral lipid fatty acid mycorrhizal biomarker, C16:1cis11. Identification of AMF-promoting cover crops for inclusion in diversified, no till cropping rotations in the upper Midwest U.S. will provide opportunity for reduced inorganic nutrient application with economic and environmental benefit.