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International Journal of
Environmental Research
and Public Health
Review
Potential for Mycorrhizae-Assisted Phytoremediation of
Phosphorus for Improved Water Quality
Jessica A. Rubin * and Josef H. Görres
Citation: Rubin, J.A.; Görres, J.H.
Potential for Mycorrhizae-Assisted
Phytoremediation of Phosphorus
for Improved Water Quality. Int. J.
Environ. Res. Public Health 2021,18, 7.
https://dx.doi.org/doi:10.3390/
ijerph18010007
Received: 24 September 2020
Accepted: 14 December 2020
Published: 22 December 2020
Publisher’s Note: MDPI stays neu-
tral with regard to jurisdictional claims
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affiliations.
Copyright: © 2020 by the authors. Li-
censeeMDPI, Basel, Switzerland. This
articleis an open accessarticle distributed
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Creative CommonsAttribution(CC BY)
license(https://creativecommons.org/
licenses/by/4.0/).
Plant and Soil Science, University of Vermont, Burlington, VT 05405, USA; jgorres@uvm.edu
*Correspondence: Jessica.Rubin@uvm.edu; Tel.: +1-802-839-8286
Abstract:
During this 6th Great Extinction, freshwater quality is imperiled by upland terrestrial
practices. Phosphorus, a macronutrient critical for life, can be a concerning contaminant when
excessively present in waterways due to its stimulation of algal and cyanobacterial blooms, with
consequences for ecosystem functioning, water use, and human and animal health. Landscape
patterns from residential, industrial and agricultural practices release phosphorus at alarming rates
and concentrations threaten watershed communities. In an effort to reconcile the anthropogenic
effects of phosphorus pollution, several strategies are available to land managers. These include
source reduction, contamination event prevention and interception. A total of 80% of terrestrial plants
host mycorrhizae which facilitate increased phosphorus uptake and thus removal from soil and water.
This symbiotic relationship between fungi and plants facilitates a several-fold increase in phosphorus
uptake. It is surprising how little this relationship has been encouraged to mitigate phosphorus for
water quality improvement. This paper explores how facilitating this symbiosis in different landscape
and land-use contexts can help reduce the application of fertility amendments, prevent non-point
source leaching and erosion, and intercept remineralized phosphorus before it enters surface water
ecosystems. This literature survey offers promising insights into how mycorrhizae can aid ecological
restoration to reconcile humans’ damage to Earth’s freshwater. We also identify areas where research
is needed.
Keywords:
mycorrhizae; phosphorus; water quality; mycoremediation; phytoremediation; ecological
restoration; ecological reconciliation; myco-phytoremediation; symbiosis
1. Introduction
1.1. Worldwide Freshwater Quality Threats
Currently, worldwide freshwater health is increasingly threatened by unprecedented
human, terrestrial, upland practices [
1
–
5
] and global climate change [
6
]. Drinking water
and recreational resources are contaminated by emissions from non-point sources with
various management practices [
1
,
3
,
4
,
6
]. Human settlements, industries and agriculture
are the major sources of water pollution, contributing 54%, 8% and 38%, respectively [
7
].
This is especially concerning because water use is predicted to approach one-half of Earth’s
capacity by mid-century [
2
] and any contamination may reduce the utility of these resources
further. While many nutrients and pollutants are exported to water bodies through runoff,
phosphorus (P), a limiting nutrient in freshwater ecosystems, is of particular concern
because it is a non-renewable resource essential to crop production [
8
], which when
excessively discharged from landscapes can have damaging effects on the ecology of
freshwater lakes and streams. Soluble reactive phosphorus (SRP) stimulates the growth
of algal and toxic cyanobacteria [
9
,
10
], causing eutrophication, which results in anoxic
conditions [
11
–
13
], directly harming human and animal health [
14
]. While most of the
solution lies in evolving upland practices, ecological engineering offers creative ways
that recover and recycle phosphorus upland, supporting food security while mitigating
eutrophication [15].
Int. J. Environ. Res. Public Health 2021,18, 7. https://dx.doi.org/10.3390/ijerph18010007 https://www.mdpi.com/journal/ijerph
Int. J. Environ. Res. Public Health 2021,18, 7 2 of 23
1.2. Relatively New Field of Myco-Phytoremediation
Though the role of fungi in ecosystem processes has long been recognized, mycore-
mediation is considered an emerging field. Bioremediation technologies, that originally
harnessed bacteria to mitigate pollutants, have been a crucial tool in the last 60 years to
filter contaminants from wastewater before discharge to surface water. Now, bioremedia-
tion involves a much wider group of organisms including fungi. Mycoremediation can
serve as a mitigation approach for non-point source pollution that addresses the problem
through source reduction, contamination event prevention, and pollutant interception
upland of the receiving water body [
16
]. Research on mycoremediation has involved
enhanced rhizosphere cycling and mineralization of heavy metals, pharmaceutical wastes,
polycyclic hydrocarbons, agricultural wastes (pesticides and herbicides), phthalates, dyes,
and detergents, when working in tandem with microbes [
17
]. Absent from this list is
phosphorus, a ubiquitous agricultural pollutant of freshwater bodies. Given the role of P
in water quality degradation, it is surprising that mycorrhizal fungi have not been used in
repairing landscapes to facilitate P uptake from soil and thereby preventing it from loading
to water bodies.
Phytoremediation, on the other hand, involves plants that remove various pollutants such
as hydrocarbons, alkanes, phenols, polychlorinated solvents, pesticides, chloroacetamides,
explosives, trace elements, toxic heavy metals, metalloids and landfill leachates [
18
,
19
].
Phytoremediation is a cost-effective and environmentally sound way to conserve soil and
water resources as well as provide farmers with viable hay for their livestock [
20
] and other
resources. Phytoremediation could be enhanced with appropriate arbuscular mycorrhizae
fungi (AMF) [
21
] and ectomycorrhizae (ECM). Plant uptake can reduce P concentrations in
soil solution and thus reduce the movement of dissolved P into surface waters.
When mycoremediation and phytoremediation are combined, a synergistic symbiosis
is facilitated which also includes microbes [
22
,
23
]. In the literature, the reported utility is in
remediating metals and PCBs [
24
–
27
]. To our knowledge, it has not yet been applied to P
mitigation rigorously beyond pilot projects, hence case studies are few and far between.
1.3. Mycorrhizae
Mycorrhizae fungi are 400 million-year-old ecological engineers whose evolutionary
success has been attributed to their ability to expand the rhizosphere of plants, enabling
greater uptake of nutrients from surrounding soils [
28
]. Early research indicates mycorrhizal
application in agricultural production reduces the amount of P fertility amendments required
for plant growth, tantamount to source reduction. Influx of P in roots colonized by mycor-
rhizal fungi can be 3–5 times higher than in non-mycorrhizal roots [
29
]. Their effectiveness
in agricultural landscapes, however, is variable given the wide variety of farm management
systems and other factors that interfere with their success. Rillig et al. [
30
] advocates for the
development of mycorrhizal technologies to enhance agroecosystems sustainably.
Mycorrhizal fungi are keystone mutualists in terrestrial ecosystems [
31
] whose ecolog-
ical role in assisting recovery of severely disturbed ecosystems [
18
] is evident because they
enhance P plant uptake in both crops and woody plants. Thus they could play an important
role in myco-phytoremediation of phosphorus. This involves ecosystem engineering which
harnesses nutrient exchange networks crucial to ecosystem succession and resilience [
32
].
This strategy, though still relatively novel in modern landscapes, has tremendous potential
to be applied in the burgeoning field of reconciliation ecology [
33
], which acknowledges
that, while ecosystems cannot be completely restored to their original state, they can be
reestablished to reverse their degradation to return to a new balance [34].
Of the seven groups of mycorrhizae, the two most common in agricultural and forested
lands [
28
] are also the most likely to be employed in myco-phytoremediation: AMF and
ECM. While AMF and ECM provide similar services to the plant (i.e., improved access to
P) [
29
], their hyphae differ in architecture and in how they transfer P to the plant [
35
]. In the
AMF, the transfer is accomplished intercellularly and via intracellular arbuscules from
extra-radical hyphae that extend directly into the soil beyond plant rhizosphere depletion
Int. J. Environ. Res. Public Health 2021,18, 7 3 of 23
zones [
36
]. In ECM, the transfer occurs via intercellular Hartig net hyphal networks
surrounding epidermal and cortex cells while outside of the mantle, extra radical mycelia
form extensive nutrient-absorbing networks in the soil [
37
,
38
]. It is well established that
AMF and ECM greatly enhance the uptake of immobile soil nutrients such as P by plant
root hosts [
35
,
39
,
40
] and improve soil properties. They also increase below- and above-
ground biodiversity and provide pathogen resistance. This results in improved tree and
shrub survival, better growth and establishment on moisture-, nutrient- and salt-stressed
soils [
41
–
44
]. In addition, they facilitate plant succession [
45
,
46
]. Mycorrhizae growing
around or in roots utilize carbohydrates from the host, and in return supply the host with
P [29], water and other nutrients [47,48].
Additionally, when planting into AMF grasslands, tree and shrub species’ growth
and survival is improved by inoculation with ECM specific to the species planned [
49
].
ECM presence can support native trees to endure aggressive non-native species’ pres-
ence [
50
] as well as play a critical role in the restoration of degraded sites [
48
]. Mycorrhizae
can assist in decreasing P pollution in each component of the three-pronged strategy
introduced above: source reduction via decreasing P amendment amounts needed, con-
tamination event reduction by decreasing erosion through improved soil structure and
vegetation establishment and pollutant interception via redirecting P into plant roots out
of soil and water.
This paper provides an overview of current research on how mycorrhizae and their
native hosts can mitigate water quality degradation. In researching the application of
mycorrhizae to remediate phosphorus for water quality purposes, we found ample studies
investigating mycorrhizal symbioses in crops such as sorghum, wheat, corn, clover [
51
]
but few studies applying them specifically to address water quality issues. The scope
of this paper is limited to P mitigation in agricultural and urban settings mainly within
temperate climate regions. In particular, we present a survey of literature which highlights
mycorrhizal services that would potentially be of utility in myco-phytoremediation of P in
the context of best management practices for water quality improvement across landscapes.
Different research fields use different terminologies for P species. We use SRP to mean
the dissolved inorganic phosphorus pool, i.e., plant available orthophosphate. Inorganic
phosphate includes this pool but also the adsorbed portion and precipitates of phosphate.
2. The Phosphorus Problem
Most P enters water bodies as non-point source pollution with overland flow and
streambank erosion of legacy P [
52
] and from leaching of long-term barnyard manure-
amended soils [
53
]. The urgency to address this is not only due to the increasing eutrophi-
cation of waters around the world but also due to the finite P resources that remain and
the presence of abundant legacy phosphorus, accumulated in soils from past fertilizer and
manure inputs. Legacy P resources could substitute manufactured fertilizers, preserve
the finite phosphate rock reserves and gradually improve water quality [
54
]. Additional
urgency is due to the fact that water quality improvement will be gradual as a result of
the inherent lag time between the initiation of P mitigation and tangible water quality
outcomes. These lag times can be attributed to the chronic and continual release of non-
point source pollution (NPS) from soils enriched in P during past management [
55
,
56
].
For this reason, NPS watershed mitigation projects often fail to meet expected timetables for
water quality improvement [
57
]. When managing for P mitigation, it is helpful to identify
whether mitigation practices focus on total P (TP) or SRP. Technically, both are important:
in deep lakes, bioavailable P is more threatening to water quality health, whereas the
impact of particulate P is more significant in shallow waters, due to its resuspension ability.
However, well-intentioned conservation measures that reduce particulate P (PP) losses are,
they may unintentionally contribute to increases in ecologically damaging SRP loads [
58
].
This emphasizes the importance of paying attention to P speciation (organic P ranging from
35 to 70% [
59
]) in conservation practices. SRP is important to study separately from TP
Int. J. Environ. Res. Public Health 2021,18, 7 4 of 23
because this portion is immediately bioavailable in contrast to P associated with sediment
or organic matter [60].
Typical sources of phosphorus are manure, fertilizer and compost, although P is also
naturally present in soil minerals such as apatite [
61
]. Because manure and composts are
often enriched in P relative to nitrogen and the stoichiometry of plant needs [
62
], P builds
up in soils, which may lead to P saturation [
63
]. The phosphorus cycle is complex and
there are soils that have vast reserves of total P that can exceed SRP 100-fold [64].
Hence a key challenge is how to raise the efficiency of agriculture to increase the
availability of inorganic phosphorus (Pi) soil reserves to crop plants [
65
] while also reducing
inputs. In agricultural soils, P use efficiency is low compared to the amount that is adsorbed
to soil colloids where it is strongly held. Although P is rendered less mobile by sorption,
it finds its way into water courses mainly by erosion of phosphorus-laden sediments [66].
A phosphorus source reduction approach involves meeting sufficiency recommenda-
tions based on soil tests [
67
,
68
]. Calculations of P removal as a function of crop, soil and
management factors differentiate areas that may vary in P soil test levels (and resulting
potential for P runoff). Doing so can inform large-scale applications using the P site index
where P soil test levels cannot be determined for each specific tract of land [69].
Another strategy to reduce P fertilizer use, not often considered in soil fertility mea-
surements, is to involve soil structure improvement that would increase organic matter
storage and thus P storage which could become available to plants [
70
]. P sorption maxima
have been correlated with carbon (C) from organic matter due to humic Fe, Al complexes
responsible for increased P sorption [71].
Plants invest up to 20% of photosynthate in mycorrhizal symbioses [
72
] to obtain nutri-
ents whose available forms are in short supply [
28
]. The mechanism by which mycorrhizae
enhance nutrient uptake is through extending reach of plant roots via extensive hyphal
networks, which can exceed distances of 11 cm from the host root [
73
], or by manipulating
the chemical environment to release more phosphate from labile organic and inorganic
sources [74,75].
3. Processes in the Phosphorus Cycle Where Mycorrhizae Affect P Availability
Mycorrhizae participate in the main P cycling processes. A simplified version of
the soil P cycle is depicted in Figure 1and shows where mycorrhizae may influence the
cycle. At the center of the cycle is orthophosphate in soil solution, also known as dissolved
or soluble phosphorus or SRP. P in this pool comprises three bio-available species of
the phosphate ion (H
2
PO
4−
, HPO
42−
, and PO
43−
). This pool is connected to all other
compartments: vegetation, organic P, P sorption sites on Fe and Al oxides, and mineral
compounds, so called secondary minerals, which form by precipitation of phosphate
with Fe, Al, and Ca ions and release phosphate by dissolution. In addition, there is a
phosphorus pool associated with primary P minerals (apatite) which releases P slowly and
which may also be manipulated by ECM [
76
]. One could further split both the organic
and the inorganic pools into two types of P: labile, fast-cycling and stable, slow-cycling P.
The efficacy of mycoremediation via mycorrhizae may rely on catalyzing these pools to
accelerate P extraction by plants which can subsequently be harvested to remove some P
from the site. This form of mitigation is called myco-phytoremediation.
Int. J. Environ. Res. Public Health 2021,18, 7 5 of 23
Int. J. Environ. Res. Public Health 2020, 17, x FOR PEER REVIEW 8 of 23
Figure 1. Influence of mycorrhizae on phosphorus cycling processes and pools. Red and green arrows are processes influ-
enced by mycorrhizae. Broken lines show the net direction of reactions due to mycorrhizal effects.
Mycorrhizal fungi affect the P cycle by several mechanisms which can be understood
as physical and biochemical. On the physical side, mycorrhizal hyphae increase the
chance that dissolved phosphate is encountered by increasing diffusion of orthophos-
phate in solution into the root–hyphal network. There are several factors that contribute
to this effect [77]: (i) AMF diameters are smaller than plant roots thereby increasing sur-
face area to access a greater soil volume [73] than plant roots alone and reducing the dif-
fusion distance; (ii) the constant turnover and new growth of AMF maximizes soil exploi-
tation [78]; (iii) AMF with high affinities for P uptake, are highly efficient [79]; and (iv)
once taken up by AMF hyphae, orthophosphate is converted into polyphosphate, which
helps maintain a phosphate concentration gradient across the soil–hyphae boundary, as-
sisting in P uptake [80]. Here it is helpful to consider the spatial distribution of P pools
and their relationship to the distribution networks of roots and hyphae (Figure 2). On the
one hand, the root–hyphae partnership has to compete for solution phosphate with mi-
crobial immobilization, sorption and precipitation. On the other hand, mineralization, de-
sorption and dissolution locally liberate phosphate into soil solution; hyphae increase the
chance that plants have agents in the place and at the time where and when these events
occur (Figure 2).
Mycorrhizae-associated biochemical processes that increase plant uptake involve or-
ganic acids [81] that dissolve precipitates of phosphates and primary minerals [74] and
phospholytic enzymes that help mineralize P from organic sources [82]. Recently it has
been recognized that mycorrhizae may act in concert with other microorganisms in their
mycorrhizosphere [76,77] to increase phosphate mineralization [83] similar to enhanced
mineralization in the rhizosphere [81]. Biochemical processes can differ from the physical
processes because they allow hyphae to take up phosphate directly from the organic res-
idues, thus bypassing soil solution (green arrow in Figure 1). This may have important
consequences for myco-phytoremediation (explained more below) as it releases plants
from competition for P by adsorption and precipitation.
Erosion control is an effective way to prevent the movement of sediment-bound P
into water bodies [84]. This is noteworthy since mycorrhizae affect soil structure on both
micro and macroscopic levels. AMF produce glycoprotein glomalin, which binds soil par-
ticles into aggregates [85], remaining in the soil even after mycorrhizal death [86]. The
increased aggregation reduces erosion by maintaining a porous yet stable soil structure
[87]. Greater ECM activity can increase stable aggregate levels in the soil due to fungal
Figure 1.
Influence of mycorrhizae on phosphorus cycling processes and pools. Red and green arrows are processes
influenced by mycorrhizae. Broken lines show the net direction of reactions due to mycorrhizal effects.
Mycorrhizal fungi affect the P cycle by several mechanisms which can be understood
as physical and biochemical. On the physical side, mycorrhizal hyphae increase the chance
that dissolved phosphate is encountered by increasing diffusion of orthophosphate in
solution into the root–hyphal network. There are several factors that contribute to this
effect [
77
]: (i) AMF diameters are smaller than plant roots thereby increasing surface area
to access a greater soil volume [
73
] than plant roots alone and reducing the diffusion dis-
tance; (ii) the constant turnover and new growth of AMF maximizes soil exploitation [
78
];
(iii) AMF with high affinities for P uptake, are highly efficient [
79
]; and (iv) once taken
up by AMF hyphae, orthophosphate is converted into polyphosphate, which helps main-
tain a phosphate concentration gradient across the soil–hyphae boundary, assisting in P
uptake [
80
]. Here it is helpful to consider the spatial distribution of P pools and their
relationship to the distribution networks of roots and hyphae (Figure 2). On the one hand,
the root–hyphae partnership has to compete for solution phosphate with microbial immo-
bilization, sorption and precipitation. On the other hand, mineralization, desorption and
dissolution locally liberate phosphate into soil solution; hyphae increase the chance that
plants have agents in the place and at the time where and when these events occur (Figure 2).
Mycorrhizae-associated biochemical processes that increase plant uptake involve
organic acids [
81
] that dissolve precipitates of phosphates and primary minerals [
74
] and
phospholytic enzymes that help mineralize P from organic sources [
82
]. Recently it has
been recognized that mycorrhizae may act in concert with other microorganisms in their
mycorrhizosphere [
76
,
77
] to increase phosphate mineralization [
83
] similar to enhanced
mineralization in the rhizosphere [
81
]. Biochemical processes can differ from the physical
processes because they allow hyphae to take up phosphate directly from the organic
residues, thus bypassing soil solution (green arrow in Figure 1). This may have important
consequences for myco-phytoremediation (explained more below) as it releases plants
from competition for P by adsorption and precipitation.
Int. J. Environ. Res. Public Health 2021,18, 7 6 of 23
Int. J. Environ. Res. Public Health 2020, 17, x FOR PEER REVIEW 8 of 23
hyphae growth [88] thereby enhancing soil restoration, driving plant community devel-
opment [89], and hence can serve as a management tool to support restoration of boreal
and temperate forest ecosystems [48] which includes buffers and vegetated drainageways.
Figure 2. Interactions among spatially distributed organic, adsorbed, and particulate mineral phosphorus microsites, soil
Scheme 4. and mycorrhizae hyphae.
A crucial task in P runoff mitigation is to accelerate P removal from where it has
accumulated, over years of agricultural management, in crop fields, pastures, and buffers.
This task can be aided by mycorrhizae through three steps: P uptake via mycorrhizae, P
acquisition from the soil into storage, and P allocation to places in the plant where it is
needed (Figure 3) [90,91]. Plant processes such as modifications in root structure, organic
acid, proton, and phosphate production and activation of high affinity transporters affect
P acquisition [92] as do mycorrhizae associations [93]. P utilization efficiency meanwhile
is governed by P transport within the plant remobilization and internal P apportionment
to maintain plant metabolism under low P concentrations [94,95]. It is important to note
that these processes occur at spatially distributed microsites in the soil as shown in Figure
2.
Figure 3. Multistep transfer of orthophosphate from soil through mycorrhizae to the plant.
Figure 2.
Interactions among spatially distributed organic, adsorbed, and particulate mineral phos-
phorus microsites, soil Scheme 4 and mycorrhizae hyphae.
Erosion control is an effective way to prevent the movement of sediment-bound P
into water bodies [
84
]. This is noteworthy since mycorrhizae affect soil structure on both
micro and macroscopic levels. AMF produce glycoprotein glomalin, which binds soil
particles into aggregates [
85
], remaining in the soil even after mycorrhizal death [
86
]. The
increased aggregation reduces erosion by maintaining a porous yet stable soil structure [
87
].
Greater ECM activity can increase stable aggregate levels in the soil due to fungal hyphae
growth [
88
] thereby enhancing soil restoration, driving plant community development [
89
],
and hence can serve as a management tool to support restoration of boreal and temperate
forest ecosystems [48] which includes buffers and vegetated drainageways.
A crucial task in P runoff mitigation is to accelerate P removal from where it has
accumulated, over years of agricultural management, in crop fields, pastures, and buffers.
This task can be aided by mycorrhizae through three steps: P uptake via mycorrhizae,
P acquisition from the soil into storage, and P allocation to places in the plant where it is
needed (Figure 3) [
90
,
91
]. Plant processes such as modifications in root structure, organic
acid, proton, and phosphate production and activation of high affinity transporters affect P
acquisition [
92
] as do mycorrhizae associations [
93
]. P utilization efficiency meanwhile is
governed by P transport within the plant remobilization and internal P apportionment to
maintain plant metabolism under low P concentrations [
94
,
95
]. It is important to note that
these processes occur at spatially distributed microsites in the soil as shown in Figure 2.
Mycorrhizospheres and their composition significantly affect the mobilization of both
inorganic particulate and organic P into the SRP pool. This depends on both the quality
and the concentration of acids released by mycorrhizae [
96
]. Mycorrhizal fungi and roots
also transport nutrients considerable distances [97].
The amount of SRP in the soil solution affects the efficacy of mycorrhizae to enter
into symbiosis with the plant [
98
,
99
]. Increased SRP has inhibitory effects on development
of external hyphae in soil core experiments [
100
] and thus the AMF are less likely to
improve scavenging for P. In contrast when SRP is low, mycorrhizal infections and hyphal
growth increase [
101
] resulting in greater plant P uptake and thus less chance of leaching
of SRP [100].
In comparison to the sum of the other pools, soil solution phosphorus (SRP) can
constitute as little as 0.1% of TP [
64
,
102
,
103
]. This is exacerbated by the fact that sorption
rates of P are generally greater than plant uptake [
104
–
106
]. Thus newly applied phosphate
becomes unavailable quickly, triggering the need for more P fertilization [
107
]. For this
reason, agronomic assessments of plant available P have focused primarily on sorption-
desorption and precipitation-dissolution [
108
]. The sorption-desorption reaction and the
precipitation-dissolution reactions are equilibrium reactions. Thus, when the concentration
Int. J. Environ. Res. Public Health 2021,18, 7 7 of 23
of phosphate in soil solution is reduced by microbial immobilization and plant uptake,
the two labile inorganic pools supply phosphate to maintain the partitioning ratio of solid
phase to dissolved phase. In the presence of mycorrhizae, soil solution may then become a
‘pipeline’ for accelerated removal of P from the mineral pools to the plant.
Int. J. Environ. Res. Public Health 2020, 17, x FOR PEER REVIEW 8 of 23
hyphae growth [88] thereby enhancing soil restoration, driving plant community devel-
opment [89], and hence can serve as a management tool to support restoration of boreal
and temperate forest ecosystems [48] which includes buffers and vegetated drainageways.
Figure 2. Interactions among spatially distributed organic, adsorbed, and particulate mineral phosphorus microsites, soil
Scheme 4. and mycorrhizae hyphae.
A crucial task in P runoff mitigation is to accelerate P removal from where it has
accumulated, over years of agricultural management, in crop fields, pastures, and buffers.
This task can be aided by mycorrhizae through three steps: P uptake via mycorrhizae, P
acquisition from the soil into storage, and P allocation to places in the plant where it is
needed (Figure 3) [90,91]. Plant processes such as modifications in root structure, organic
acid, proton, and phosphate production and activation of high affinity transporters affect
P acquisition [92] as do mycorrhizae associations [93]. P utilization efficiency meanwhile
is governed by P transport within the plant remobilization and internal P apportionment
to maintain plant metabolism under low P concentrations [94,95]. It is important to note
that these processes occur at spatially distributed microsites in the soil as shown in Figure
2.
Figure 3. Multistep transfer of orthophosphate from soil through mycorrhizae to the plant.
Figure 3. Multistep transfer of orthophosphate from soil through mycorrhizae to the plant.
Certain agricultural management practices such as avoiding overfertilization, and ap-
plying soil microorganisms which enhance P uptake like mycorrhizae fungi can move us
toward more efficient P use [
109
]. Other strategies may rely on plants that utilize P more
efficiently by selecting cultivars, plant breeding or genetic engineering [110].
The host plant’s P requirement and level of soil available P will also influence the
extent of plant response to mycorrhizae [
111
]. AMF partners with 85% of plant families and
can achieve a several-fold increase in plant uptake of phosphate compared to plants lacking
these associations [
36
,
83
,
112
]. However, there is a wide spectrum of P uptake efficiency
that can be attained by different AMF species [
113
,
114
]. Greater diversity of AMF is linked
with ecosystem productivity and total P uptake potentially because different soil niches are
occupied by different species [114].
Soil solution may not be the only source of P for AMF. The idea that this group of
mycorrhizae might be saprotrophic [
115
] (i.e., they participate directly in the decomposition
of organic matter to obtain carbon) is receiving renewed interest [
116
]. Mobilization of
phosphate from organic matter may be a direct effect of the release of acid phosphatase [
82
].
However, other mechanisms have also been invoked. Mycorrhizae may prime or stimulate
bacteria that live in the mycorrhizosphere by providing some of the photosynthate supplied
by the plant [117]. Some species can also hydrolyze organic P compounds [118].
Increased plant uptake has been linked to reduction in phosphate leaching in several
studies with AMF and thus has a direct effect on water quality. Zhang et al. [
119
] showed
that SRP was reduced in both leachate and runoff by 11% and 81%, respectively. That
study also found that losses of PP and dissolved organic P from rice mesocosms were
much larger than SRP losses, but were also reduced. Bender et al. [
120
] found that AMF
reduced leaching of SRP and unreactive P (total P minus SRP) by 31% over soils without
AMF in grass mesocosms. Similar reductions with AMF were demonstrated by van der
Heijden [
121
]. Martinez-Gracia [
122
] found that regardless of rainfall intensity mycorrhizae
decreased P leaching losses by 50%. With climate change likely resulting in increased
rainfall intensity in certain areas of the earth [
123
,
124
], mycorrhizae assist in resilient
ecosystem response.
ECM is thought of as the group of mycorrhizae which can directly mineralize nutri-
ents [
115
] from organic matter by releasing extracellular phospholytic enzymes [
116
,
125
].
Though they are not as ubiquitous as AMF, they partner with 10% of plant families, mainly
Int. J. Environ. Res. Public Health 2021,18, 7 8 of 23
woody species. However, ECM also increases P uptake from soil [
74
,
126
] likely protect water
quality by conserving nutrients in forest ecosystems [115], such as riparian forested buffers.
Although mycorrhizae are strongly involved in phosphorus cycling, agricultural man-
agement affects mycorrhizal presence, abundance and effectiveness, influencing fertilizer
need [127].
4. Mycorrhizae, Landscapes and Soils
Any design of a phosphorus mitigation strategy that involves mycorrhizae has to
consider landscape position and soils which affect P availability and fate. In an ideal
agricultural landscape, production fields are separated from water courses by a forested
(or otherwise vegetated) riparian buffer [
128
], that attenuates the increased P in leachate
when high fertilizer P is applied [
129
]. Each landscape element in the catena has a different
role to play in P mitigation. Drainage class and vegetation need to be considered as
variables for establishment of mycorrhizal communities. The mycorrhizal communities
likely differ between high organic matter riparian forest including both AMF and ECM
and the agricultural field of earlier succession dominated by AMF [
130
]. Drainage class
per se may not affect mycorrhizal plant infections. In a study on soybean fields stretching
across three soil drainage classes (poorly, somewhat poorly, and moderately well drained),
more AMF spores were found in the more poorly drained than the better drained soils.
But, there was no discernible difference in colonization of plant roots [
131
]. In agricultural
systems where flooding diminishes vegetation, crops following the flood are P deficient
early in the season. The lack of hosts during flooding may result in lower colonization rates
by AMF [
132
]. Lack of vegetation during flooding is not likely to occur in forested riparian
forests [
133
] and agricultural fields can be managed to provide hosts through rotations and
cover crops [127].
However, drainage class may still enter into any myco-phytoremediation design
because prolonged flooding in wetland riparian buffer, remobilizes P adsorbed to soil
colloids. In particular, under anaerobic conditions ferric iron is reduced, releasing phos-
phate that would otherwise be strongly sorbed to feric oxides [
134
]. It is not clear whether
mycorrhizae can help with recovering P released in this way.
In terms of the water mitigation paradigm, agricultural fields would be targets of
source reduction as they are the primary recipients of P. However, in an area where
agriculture was practiced for decades, it is likely the soil has sufficient P to be a source
itself [135].
High SRP concentrations in agricultural fields are likely to reduce mycorrhizal infec-
tions [
136
]. Therefore, the amount of fertilizer P should be judicious [
137
–
139
]. Manage-
ment of agricultural lands should consider the use of alternatives to inorganic P fertilizer
to promote mycorrhizal growth and colonization [120,140].
Consequently, managing the field for mycorrhizae can reduce the amount of P fertilizer
needed to achieve yield goals [
127
]. This includes reducing tilling and maintaining hosts
by implementing crop rotation, and also choosing crops with root architecture efficient in
accessing sufficient P and forming a symbiosis with AMF [101].
Oka [
141
] found that P application on soy beans could be reduced from 150 to
50 kg P ha
−1
without yield loss when it followed wheat, an AMF mycorrhizal crop (Triticum
sativum); then when followed by radish (Raphanus sativus), a non-mycorrhizal crop. The ben-
efits may be due to better establishment of mycorrhizae–plant associations under the low
soil P supply in the early season with increased uptake of P ensuing [
142
]. Application
of excessive fertilizer at this time of the growing season may inhibit mycorrhizal infec-
tions [
142
] and should be avoided. Mycorrhizal cover crops may thus have several benefits
to the plant. First, they provide hosts for mycorrhizae and a source of organic P, scavenged
between cash crops. In addition, over time, the amount of sediment-bound phosphorus
lost by erosion will diminish. Consequently, downslope P accumulations in riparian areas
are minimized.
Int. J. Environ. Res. Public Health 2021,18, 7 9 of 23
Although agriculture can be regarded as a myco-phytoremediation system for legacy P,
agricultural practices affect mycorrhizae. The type and timing of tillage has been identified
as one such factor. The role of fungi in plant nutrition and soil conservation is compromised
when the formation and survival of propagules (i.e., spores, hyphae, colonized roots) are
threatened though tillage, disrupting physical and biological properties of soil. Spores
serve as “long- term” propagules when host plants are not present, whereas hyphae are the
main source of inoculum when plants are present in undisturbed soil. Deep plowing can
dilute propagules, reducing plant root inoculations, especially in autumn when hyphae are
detached from the host plant. Conservation tillage can protect survivability and inoculation,
thereby improving soil aggregation and P uptake [143].
The structure and texture of soils is also an important factor in whether AMF has
significant impacts on leaching and erosion. In agriculture, it is important to look at the
relationship between fertilization and runoff. AMF significantly reduced nutrient leaching
after rainfall events in sandy grassland soils [
121
]. This research has important implications
for soils with poor P sorption capacity such as sandy soils and other highly permeable soils
or heavily manured soils [71], where P can be lost during rainfall events.
Furthermore, mycorrhizae can intercept P in soil solution before it leaves the root zone
with deep percolation. In contrast to the many studies that assess the effect of mycorrhizae
on plant uptake of P, only few of them report how mycorrhizae affect P leaching. This is
usually not regarded as a major pathway of P export from a field because of the high affinity
of phosphate [
144
] to soil surfaces. However, Asghari et al. [
100
] explained that sandy-
textured soils are likely to provide little internal surfaces for P adsorption. In addition, soils
that receive high P fertilizer may also leach phosphate [
129
]. Water quality in freshwater
bodies is sensitive to even small amounts of P [
145
] and thus leaching may have a significant
effect. Ashgari et al. [
100
] found that AMF can reduce leachate P from soil columns packed
with a loamy sand. In another laboratory experiment Köhl and van der Heijden [
144
] found
that the effect varied with AMF species probably due to differences in root colonization:
the more root colonization the greater the growth of the plant and presumably the less P
was leached. This is because AMF symbiosis assists plants with P uptake [
140
,
146
] through
reaching beyond P depletion zones to access greater soil P reserves [
74
]. Plant response
to mycorrhizal formation depends upon the extent of mycorrhizal development [
47
]. It is
not clear whether the results of these controlled laboratory studies are directly transferable
to processes that occur in the field where many other factors are in play; more research is
needed here.
Mycorrhizae are involved in most aspects of P cycling as can be seen in Figure 1. Data
from the literature that show the effect of mycorrhizae on plant uptake, leachate and soil
concentration. For example, plant uptake can be enhanced by between 40 and several 100 s
of percent, leachate P is reduced by up to 60% and extractable P by 15% in a growing season
(Table 1). However, variations in both plant and mycorrhizae species greatly influence P
removal from soil and leachate.
5. Riparian Buffers
It has long been recognized that a functioning riparian forest can retain nutrients
exported from agriculture [
128
]. They have been proven effective in temporarily reduc-
ing agricultural P loads through settling sediments, microbial immobilization and plant
uptake [
147
] and are associated with the recovery of impaired streams in agricultural
watersheds [148].
However, riparian watersheds have been under strong development pressure. Con-
version of these forests to cropland or grazing [
149
] has led to ecological impairment of
these areas [
150
]. As a result the earth’s waterways are threatened by widespread loss of
ecological services and functions and will require collective stewardship which involves
ecosystem based solutions and technical strategies to improve water infrastructure [
151
].
Mycorrhizae have been proposed as technologies that could help with restoration [
45
].
A greenhouse microcosm experiment involving the grass Phalaris aquatica L investigated
Int. J. Environ. Res. Public Health 2021,18, 7 10 of 23
the effects of AMF on plant growth, nutrient depletion from soil and leaching via water.
The results indicate that where P was added, P levels in both the soil and water were
significantly lower in the mycorrhizal inoculated plants compared to the non-inoculated
plants. These results suggest riparian management practices which promote mycorrhizae
could help minimize nutrient loss. What is most significant about this study is that it occurs
in Australia’s nutrient-challenged riparian ecosystems, demonstrating how increasing
this below-ground diversity can support nutrient interception in areas which experience
rapid influxes of nutrients [
112
]. In theory, mycorrhizae could access P released from
labile pools in sediments from upland soils. ECM fungi, and AMF, can directly access
organic phosphorus for the plant [
116
], thus bypassing soil solution where plants would
face intense competition for P from sorption and microbial uptake.
Plant uptake in buffers and bioretention projects can be significant, depending on plant
species, type, and age [
152
]. For example, P uptake in a riparian buffer by woody vegetation
(Populus deltoides in this case) was higher than herbaceous vegetative uptake [
152
] and
the P amount removed via harvest was 62 kg P ha
−1
over four years; 63% higher than in
a control stand of smooth brome (Bromis inermis). Willows are suggested frequently for
phytoremediation projects [
153
] because they are fast growing and can endure wet sites.
They also have increased transpiration rates [
154
], which make them good candidates for
accumulating P in their biomass.
Storage of P in buffer strips is not forever and release of P occurs at different time
scales. Release may be associated with seasonal cycles such as growing and senescence
periods of vegetation and the associated decomposition of dead plant material, and release
of phosphate from labile mineral pools during flooding events. Ultimately removal of P
has to be managed by harvesting perennial vegetation [
152
,
155
], so called phytoextraction,
to reduce or prevent remobilization of nutrients and the inevitable release of accumulated
P [
156
–
158
]. Phytoextraction is the last step of phytoremediation that directly impacts
water quality and provides economic incentives to the farmer [152,155].
Harvesting buffer zone grasses and woody biomass removes accumulated P and pre-
vents P saturation, increasing P retention and decreasing SRP losses in surface runoff [
159
].
In particular, the shrub zone tends to be the most efficacious to harvest because woody
vegetation has greater uptake potential than herbaceous vegetation [
152
]. The harvesting
of plant biomass may further ensure greater species diversity in wet areas exposed to
high levels of external nutrient loading [
160
]. Inoculation with AMF and ECM could
increase plant uptake by several fold. Some plants lend 45themselves to harvesting better
than others. Plant selection is important in all landscapes as it is in agricultural areas to
remediate terrestrial pollution. The high P uptake efficiency of willows, makes them a
prime candidate for coppicing, the cyclic removal of biomass from trees, because willows
have been documented to uptake 33% more P when they host AMF [161].
6. Green Stormwater Infrastructure
In urban and suburban landscapes, green infrastructure systems require a phytoex-
traction element to combat the inevitable P saturation which occurs over time in buffers,
constructed wetlands (CW), and bioretention systems [
162
]. Generally, only 20% of the
world’s wastewater [
163
] is treated, with even less treatment occurring in low-income
countries [
164
]. As urban areas grow, so do impermeable surfaces and hard piping sys-
tems, which increase peak flows, stormwater volumes, and pollutant loading to rivers
and streams [
156
]. To alleviate pollution loads, many US cities have implemented best
management practices (BMPs) that slow and treat runoff. Among these are measures
ranging from green roofs to constructed wetlands (CW).
Green roofs provide a range of ecosystem services such as stormwater retention,
temperature moderation, urban biodiversity, carbon sequestration, and enhanced aesthet-
ics [
157
]. It is important that leachate from green roofs be filtered and monitored [
165
]
Since P is almost universally found in higher concentrations (as much as 20 times) in
their leachate than in conventional roof runoff [
158
]. Mycorrhizae can be effectively inte-
Int. J. Environ. Res. Public Health 2021,18, 7 11 of 23
grated into green roof design to help plants endure dry and nutrient poor conditions while
providing erosion control, species diversity and nutrient mitigation [158].
Bioretention is a common BMP which involves stormwater flowing through a vege-
tated area with engineered soil mixes [
166
]. Bioretention cells help reduce peak flows and
remove pollutants such as nutrients and metals, through physical filtration, sorption, plant
uptake, and microbial reactions. A challenge with these has been that the bioretention soil
mix can become a source of nutrients and thereby contribute to water degradation [
167
].
Mesocosm experiments found that ECM and AMF mycelium in bioretention media planted
with Carex stipata reduced TP by 13–48% and SRP by 14–60% [168].
Like some riparian areas, constructed wetlands (CWs) are characterized by wet to
inundated soils. Since the 1950s, CWs have been studied as low technology methods
to treat wastewater from agriculture [
169
], residences [
170
], and industry. In domestic
wastewater, these wetlands can be effective in removing P [
13
]. Encouraging studies that
hint at the role of mycorrhizae in wetlands comes from rice paddy and CW research which
shows that even in flooded conditions mycorrhizae participate in plant P uptake [
171
,
172
].
Table 1.
The effect of mycorrhizae on plant uptake, leaching and soil P from studies carried out under different experimental
conditions and with different objectives. Underscored show the physical quantity measured.
Study Context Study Conditions Phosphorus Quantity
Measured
% Change with
Mycorrhiza #Location Ref. #
Crop uptake
Agro ecosystem
Triticum aestivum,
AMF
Phosphorus use efficiency +85–102% Uttar Pradesh,
Haryana, India [22]
Growth of native grasses
Field ecosystem and
pots in greenhouse,
Stipa pulchra Avena
barbata,
fungicide/no
fungicide ***
Shoot P concentration [mg/g]
San Diego CA,
USA [49]
Field
S. pulchra, +22%
A. barbata +68%
Greenhouse
Shoot P concentration
S. pulchra +1.6%
A. barbata −11.8%
Root concentration
S. pulchra +24%
A. barbata −15%
Mulch Experiment
Pots, greenhouse
Trifolium repens Zea
Mays Fungicide/no
fungicide ***
Plant P concentrations (%)
Morioka, Japan
[51]
No Mulch +28%
Living Mulch +135%
Plant P (mg P/plant)
No mulch +17%
Living mulch +709%
Crop uptake Pots, AMF, Allium
fistolosum
Plant P concentration [mg/g] +194% Haguromachi,
Japan [82]
Plant uptake [mg P/pot] +1525%
Effect of
mycorrhizosphere
bacteria on plant uptake
Pots, corn (Zea
Mays), AMF
P plant uptake [mg P/pot]
Denmark [83]
Shoots +168%
Roots +234%
Effect of sewage sludge P
on plant uptake
Pot, greenhouse
Glycine max AMF
Shoot biomass P [mg/shoot]
Ohio, USA [99]
No P addition +144%
150 mg P/kg addition +125%
270 mg P/kg addition −0.8%
420 mg P/kg addition −16.9%
Int. J. Environ. Res. Public Health 2021,18, 7 12 of 23
Table 1. Cont.
Study Context Study Conditions Phosphorus Quantity
Measured
% Change with
Mycorrhiza #Location Ref. #
Effect of AMF on P
leaching
Packed columns,
greenhouse, Trifolium
subterraneum AMF
Leachate P [mg]
South Australia
[100]
without added P −60%
with added P. 0%
Plant P [mg]
without added P +251%
with added P −23%
Effect of mycorrhizae on
crop uptake and
extractable soil P
Pot, greenhouse,
corn (Zea Mays),
AMF
Plant uptake (mg P/plant)
Quebec
Canada [101]
Hybrid
P3979 +8.4%
LRS +19.1%
LNS +19.8%
Mehlich 3 extractable Soil P Concentration [mg/kg]
Hybrids, no P fertilizer
P3979 −5.1%
LRS −14.4%
LNS −10.5%
Mehlich 3 extractable Soil P Concentration [mg/kg],
Hybrids, P fertilizer
applied ns
Leaching mitigation Pots, greenhouses,
Phalaris aquatic, AMF
Shoot P content (mg) +150% Southeastern
Australia [112]
Root P content (mg) +168%
Spatial differences in P
uptake between AMF
species
Pots, Medicago
trunculata, AMF
Plant P concentrations
Roskilde,
Denmark [113]
Glomus caledonium
Shoot
35 days +39%
49 days −17%
Roots
35 days +61%
49 days +10%
Scutetllospora calosporia
Shoot
35 days +39%
49 days −12%
Roots
35 days +84%
49 days +40%
Differential effect of
AMF species
Pots, Medicago
tranculata, AMF ##
P uptake [mg/plant]
Mallala, South
Australia [114]
Glomus mossae
4 weeks +1425%
8 weeks +314%
Glomus claroideum
4 weeks +625%
8 weeks +193%
Glomus intraradices
4 weeks +925%
8 weeks +357%
P losses from field Microcosms Orya
sativa L AMF
Leachate [kg P/ha] ###
Jiangsu, China [119]
Particulate P −11.1%
Dissolved Organic P −14.4%
SRP (PO4)*−81%
Runoff [kg P/ha]
Particulate P −11.1%
Dissolved Organic P −4.95%
SRP (PO4)*−11%
Int. J. Environ. Res. Public Health 2021,18, 7 13 of 23
Table 1. Cont.
Study Context Study Conditions Phosphorus Quantity Measured % Change with
Mycorrhiza #Location Ref. #
Nutrient cycling in
presence of
mycorrhizae
Microcosms, Heath
and Pasture
communities, AMF
P in leachate [mg] ###
Switzerland
[120]
Pasture
Added NH4−14.2%
Added NO3−38.5%
Heath
Added NH4−68.4%
Added NO3−63.4%
Leaching from
grasslands
Mesocosms,
grassland, AMF
Reduction in leaching
[121]
Low nutrient availability ~ 60%
High nutrient availability ns
Climate Change
Resilience
Mesocosms,
grassland
communities, AMF
Leachate P [ug] ### The Nether-
lands [122]
Moderate rain −149%
High rain −58%
Crop Uptake
Pots, Allium
fistulosum (Welsh
Onion) AMF
Shoot concentration +88% Tozawa,
Japan [127]
Crop uptake Agroecosystem
Zea Mays AMF
Plant P [mg/plant] **
Quebec,
Canada [128]
Year 1 Sample days
22 +26.5%
48 +46.5%
72 +18.7
Year 2 Sample days
22 +19.4%
48 +14.2%
72 +41.8%
Nutrient Leaching
Laboratory
mesocosms.
Lolium multiflorum,
Trifolium pratense,
sterilized soils
AMF
Leachate Loss SRP [mg]
Zürich,
Switzer-
land
[129]
Lolium multiflora
Claroideoglomus claroideum +14.2%
Funnelformis mosseae −19.5%
Rhizoglomus irregular +45.0%
Trifolium pretense
Claroideoglomus claroideum ns
Funnelformis mosseae ns
Rhizoglomus irregular ns
Unreactive P
Lolium multiflora
Claroideoglomus claroideum −10.8%
Funnelformis mosseae +3.9%
Rhizoglomus irregular ns
Trifolium pratense
Claroideoglomus claroideum +29.9%
Funnelformis mosseae +19.1%
Rhizoglomus irregular +62.4%
Vegetative buffers Pot, Salix, Populus
AMF P stem content +33%
Southern
Quebec,
Canada
[162]
Bioretention
Field mesocosms,
Carex stipata,
AMF/ECM
commercial mix
Leachate mass rate (mg/hour) ### −34%
Portland,
Oregon,
USA
[169]
Int. J. Environ. Res. Public Health 2021,18, 7 14 of 23
Table 1. Cont.
Study Context Study Conditions Phosphorus Quantity Measured % Change with
Mycorrhiza #Location Ref. #
Crop uptake Microcosms, Orya
sativa L. AMF
Plant P concentrations {mg/g] ###
Sweden [171]
First growth stage
Leaf ns
Stem +66%
Continuous flooding
No flooding −19%
ns = no significant difference; calculation of % change = (treatment
−
control)/control; ## also used leeks, but P uptake was 0, leaving
the % change undefined; ### digitized from graphs using Image J (NIH, Bethesda, Maryland); ++ only the effect of AMF considered; * %
difference represents an approximate estimate due to difficult digitization for PO
4
. Authors state that the differences were significantly
different; ** data analyzed for unfertilized plots, fungicide treatment used as control; *** treatments consisted of fungicide (no to low
mycorrhizal colonization) and no fungicide (high mycorrhizal colonization).
7. Summary of Research Results from the Literature
Table 1shows the effect of mycorrhizae on a number of the P pools and cycling pro-
cesses as reported in the literature cited above. There are several effects. First, mycorrhizal
infections clearly cause an increase in plant biomass P [
49
,
51
,
82
,
83
,
112
,
114
,
127
]. However,
in a companion greenhouse and field fungi exclusion experiment [
49
] where fungicide was
applied to inhibit mycorrhizae, the results were not as clear cut. Two grass species, Avena
barbata and Stipa pulchra, were used in this experiment. For Avena barbata, the shoot and root
concentrations were diminished by the presence of mycorrhizae in the greenhouse, but not
in the field experiment. Yet, the data showed consistently that for Stipa pulchra, P concen-
trations were greater in the mycorrhizal treatment regardless of the experimental setting.
It is not clear whether these inconsistent results are artifacts of using a fungicide. However,
the negative effects of mycorrhizae on plant P have also been reported by others for certain
experimental conditions. These include large additions of P in sewage sludge [
99
] when
additions exceeded 200 mg P/kg soil. Similarly, in an experiment with and without P
additions, Trifolium subterraneum took in less P with mycorrhizae present when P was
added [
100
]. This is in agreement with the concept that high concentrations of P may
reduce mycorrhizal infection. Duration of experimental incubation also seemed to have
been a factor in the response of P concentration in Medicago trunculata. At longer incubation
periods, the effect of both root and shoot P were less after 49 than 35 days. The effect of
mycorrhizal presence was negative for shoots after 49 days [
113
]. In another experiment,
the effect of mycorrhizae was positive on total plant P (Zea mays) [
128
] throughout the
growing season during a field study. Overall, however, mycorrhizae have positive effects
on plant P uptake.
The effect of increased plant P uptake should translate into reduced soil P if no
additional fertilizer is added. Because of the large amount of P stored, adsorbed to soil
colloids, it is difficult to detect a decrease in the total P fraction in the soil. However,
extractable P has been shown to be reduced when corn is inoculated with mycorrhizae
and is grown with no P fertilizer. This is consistent with increased P uptake by the plants.
Extractable soil P is not significantly different between mycorrhizal and non-mycorrhizal
treatments when P fertilizer is added [101].
Consequently, losses of P from the soil as leaching or runoff would also be expected
to be reduced when mycorrhizae are present. This has indeed been shown in several
laboratory column studies [
100
,
112
,
119
,
121
,
129
]. Again, the amount of soil P differentiates
the response of the plant–mycorrhizal association. In cases where P is more abundant, the
effect of the mycorrhizae on leaching is less than when P concentrations are lower [
100
,
121
].
In one study, however, leaching losses of SRP increased or were the same when mycorrhizae
were present [
129
]. In this same study, the pairing of plant species with mycorrhizal
species also affected leaching. For example, in the combination of Lolium multiflora and
mycorrhizae Rhizoglomus irregular, leaching increased by 45%, but for its combination with
mycorrhizae Funnelformis mosseae, P leaching decreased by 19.5% [
129
]. However, when
Int. J. Environ. Res. Public Health 2021,18, 7 15 of 23
Trifolium pratense was combined with three mycorrhizae, no significant differences were
observed [
129
]. Although P additions inhibited the effect of mycorrhizae on leachate P,
additions of N did not. Finally, climate change induced increases in precipitation volume
rendered the plant–fungi associations less effective in reducing P leaching, presumably
because additional rainfall creates a greater chance for more P leaching [122].
8. Research Needs
Little research has been conducted on the deliberate incorporation of mycorrhizae into
phytoremediation strategies for mitigating P loading to freshwater. In particular, research
is needed into their role in restoring riparian buffers and subsequently in the interception
of P by the mycorrhizae–plant communities. An important question in this context is “how
do mycorrhizae influence the trajectory of succession” after the initial restoration plantings.
Closely linked to this question is how much P can the plant community extract and whether
removal of plant material is feasible while facilitating ecosystem recovery. Comparing
restorations with high and low biodiversity may yield information on the efficacy of P
mitigation in buffers with these additional practices. Succession may also be affected by
the P status of the riparian area and thus the fate of any P accumulating plants [
173
] and
their mycorrhizal association.
Another promising area in need of research involves the potential of source reduction
to decrease fertilizer needs. Specific crop combinations, cover crops, and green manures
can be used to reduce fertilizer needs. Some grain crops have the ability to mobilize
P from unavailable pools and thus transfer P to subsequent crops as their residues
decompose [
165
,
174
–
176
]. Some plants with efficient P uptake may be well suited for
transfer or P from crop to crop [
177
]. These P hyperaccumulators crops include Indian
mustard, alpine pennycress, alyssum, canola, tall fescue, poplar, annual rye grass, alfalfa
and sunflower [18].
Unlike crop rotations, intercropping of P mobilizing and non-mobilizing plants [
170
,
178
]
that hyperaccumulate P may enhance removal simultaneously. Mass balance studies where
legumes, able to mobilize P, are intercropped with grains, that accumulate P, may identify
crop combinations that reduce P losses from fields. Whether P accumulation by these
plants is increased by mycorrhizae is not yet clear and merits further research. Recent
studies report improved intercrop performance, especially legume-cereal mixtures, relative
to monocrops, from enhanced P nutrition for one or more intercropped species. Research
in crop sequences and intercrops enhancing P cycling and crop nutrition, considering
crop-specific P acquisition mechanisms, microbial community action, soil property effects,
amount of and form of P will help move this promising quiver of regenerative techniques
forward for farmers to incorporate into their systems [77].
Although there seem to be some combinations of plants that can leverage the myc-
orrhizal associations for better P removal, there are examples of plants that suppress the
establishment of the symbiosis. Studies have mainly focused on invasive plants that reduce
AMF infections. For example, Himalayan impatience, Impatiens glandulifera, which has in-
vaded both European and North American riparian areas interferes with mycorrhizae [
179
].
Similarly, Reynoutria japonica, a non-mycorrhizal plant suppresses mycorrhizae and reduces
their diversity [
180
]. However, increases in mycorrhizal abundance and diversity have also
been reported for some invasions [
181
]. A general statement on the effect of invasive plants
on mycorrhizae cannot be made [182].
While there is debate about whether non-native species are ecosystem place holders
during climate change or actually malaffect native habitats and threaten ecosystem re-
silience [
183
,
184
] certain exotic species such as Phragmites australis effectively uptake excess
nutrients such as P. As a phytoaccumulator in areas of intensive vegetation [
185
] these
species can be removed annually through harvest and then used as mulch to areas seeking
more P input. Research involving this and native macrophytes which have been identified
as excellent captors of P such as Typha latifolia [186] are worthy of further study.
Int. J. Environ. Res. Public Health 2021,18, 7 16 of 23
One confounding factor in myco-phytoremediation that makes it difficult to compare
results is that currently researchers use either commercial inoculant or inoculant extracted
from the wild. There are distinctions in the effectiveness between and within these two
sources of inoculant which is not yet clearly determined. Standardized studies that compare
how commercial vs. locally gathered and propagated mycorrhizae affect P cycling may
help interpret the results of these two experimental approaches.
9. Conclusions
As 400 million-year-old symbiotic weavers of ecosystems with now 80% of terrestrial
plants, mycorrhizae hold the keys to reducing P pollution from upland accumulations.
Researching specific plant–mycorrhizae associations for P removal from soils and applying
these findings to critical source areas on farms, urban conduits, and suburban corridors
can benefit water quality.
The mycorrhizal effects that have been quantified, such as plant uptake and reduc-
tions in soil and leachate concentrations, show promise for reducing phosphorus pol-
lution by myco-phytoremediation. A holistic approach that combines source reduction,
interception, and prevention should be considered across the landscape scale. This in-
volves nutrient management based on precision farming, plant breeding, crop rotation,
intercropping, microbial engineering, microbial–fungal–floral symbiosis, increased peren-
nial green infrastructures, and deliberate harvesting. This integrated approach, known
as ‘agro-engineering’ [
54
], facilitates reconciliation of anthropogenic disturbance while
reestablishing above- and below-ground ecosystem services [187].
Mycorrhizal research in the context of water quality is scarce. Methods need to be
developed and tested to help agriculture become more regenerative and urban stormwater
infrastructure more effective. Tools are also needed which accurately assess current myc-
orrhizal presence in ecosystems to which land managers can respond accordingly. As we
develop more understanding of what AMF and ECM taxa are present and how they react
to different soil treatments, microbes and flora [
109
], a more informed use of mycorrhizae
can be brought into terrestrial landscapes to mitigate phosphorus pollution.
Author Contributions:
Conceptualization, J.A.R.; data curation, J.A.R.; J.H.G.; formal analysis,
J.H.G. and J.A.R.; funding acquisition, J.A.R. and J.H.G.; methodology, J.H.G. and J.A.R.; project
administration, J.A.R.; writing—original draft, J.A.R.; writing—review and editing, J.H.G. and J.A.R.
All authors have read and agreed to the published version of the manuscript.
Funding:
This research was funded by the USDA’s Sustainable Agricultural Research and Education
(SARE) program through a Partnership grant (#ONE19-335), the University of Vermont’s Agricultural
Research Station, the University of Vermont Center for Sustainable Agriculture, and the GUND
Institute for Environment at the University of Vermont.
Acknowledgments:
We would like to thank Terry Delaney and Daniel De Santo for their technical
assistance, the three anonymous reviewers and the Editor for their critical and constructive comments.
We acknowledge that the University of Vermont is located on unceded territory of the Abenaki people.
Conflicts of Interest: The authors declare no conflict of interest
Abbreviations
AMF Arbuscular mycorrhizal fungi also known as Endomycorrhizae
BMP Best management practices
CW Constructed wetlands
ECM Ectomycorrhizal fungi
NPS Non-point source pollution
P Phosphorus
Pi Inorganic phosphorus
PP Particulate phosphorus
SRP Soluble reactive phosphorus, orthophosphate
TP Total phosphorus
Int. J. Environ. Res. Public Health 2021,18, 7 17 of 23
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