fphys-10-00378 April 14, 2019 Time: 11:10 # 1
HYPOTHESIS AND THEORY
published: 16 April 2019
doi: 10.3389/fphys.2019.00378
Edited by:
Francesca Carella,
University of Naples Federico II, Italy
Reviewed by:
Claudio Agnisola,
University of Naples Federico II, Italy
Andrea Schievano,
University of Milan, Italy
*Correspondence:
Ellard R. Hunting
†Present address:
Casper Cusell,
Witteveen+Bos, Deventer,
Netherlands
Specialty section:
This article was submitted to
Aquatic Physiology,
a section of the journal
Frontiers in Physiology
Received: 18 June 2018
Accepted: 19 March 2019
Published: 16 April 2019
Citation:
Hunting ER, Harrison RG,
Bruder A, van Bodegom PM,
van der Geest HG, Kampfraath AA,
Vorenhout M, Admiraal W, Cusell C
and Gessner MO (2019) Atmospheric
Electricity Influencing Biogeochemical
Processes in Soils and Sediments.
Front. Physiol. 10:378.
doi: 10.3389/fphys.2019.00378
Atmospheric Electricity Influencing
Biogeochemical Processes in Soils
and Sediments
Ellard R. Hunting1,2,3*, R. Giles Harrison4, Andreas Bruder5, Peter M. van Bodegom3,
Harm G. van der Geest6, Andries A. Kampfraath6, Michel Vorenhout7, Wim Admiraal6,
Casper Cusell6†and Mark O. Gessner8,9
1School of Biological Sciences, University of Bristol, Bristol, United Kingdom, 2Biology Department, Woods Hole
Oceanographic Institution, Woods Hole, MA, United States, 3Institute of Environmental Sciences, Leiden University, Leiden,
Netherlands, 4Department of Meteorology, University of Reading, Reading, United Kingdom, 5Laboratory of Applied
Microbiology, University of Applied Sciences and Arts of Southern Switzerland, Bellinzona, Switzerland, 6Freshwater
and Marine Ecology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, Netherlands,
7MVH Consult, Leiden, Netherlands, 8Department of Experimental Limnology, Leibniz-Institute of Freshwater Ecology
and Inland Fisheries, Stechlin, Germany, 9Department of Ecology, Berlin Institute of Technology, Berlin, Germany
The Earth’s subsurface represents a complex electrochemical environment that
contains many electro-active chemical compounds that are relevant for a wide
array of biologically driven ecosystem processes. Concentrations of many of these
electro-active compounds within Earth’s subsurface environments fluctuate during
the day and over seasons. This has been observed for surface waters, sediments
and continental soils. This variability can affect particularly small, relatively immobile
organisms living in these environments. While various drivers have been identified, a
comprehensive understanding of the causes and consequences of spatio-temporal
variability in subsurface electrochemistry is still lacking. Here we propose that variations
in atmospheric electricity (AE) can influence the electrochemical environments of soils,
water bodies and their sediments, with implications that are likely relevant for a wide
range of organisms and ecosystem processes. We tested this hypothesis in field and
laboratory case studies. Based on measurements of subsurface redox conditions in
soils and sediment, we found evidence for both local and global variation in AE with
corresponding patterns in subsurface redox conditions. In the laboratory, bacterial
respiratory responses, electron transport activity and H2S production were observed to
be causally linked to changes in atmospheric cation concentrations. We argue that such
patterns are part of an overlooked phenomenon. This recognition widens our conceptual
understanding of chemical and biological processes in the Earth’s subsurface and their
interactions with the atmosphere and the physical environment.
Keywords: atmospheric electricity, bacterial respiration, biogeochemistry, Carnegie-curve, ions, redox potential
INTRODUCTION
Concentrations of various chemical compounds in surface waters, soils and sediments have been
observed to vary widely in both space and time, often detetable as diel (but also seasonal)
fluctuations (e.g., Stockdale et al., 2009;Nimick et al., 2011;Smith et al., 2011). This variability is
highly relevant for organisms that live within these spatio-temporally heterogeneous environments.
While large mobile organisms interact at broader spatial scales, small and relatively immobile
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Hunting et al. Atmospheric Electricity Links Subsurface Environments
organisms like bacteria, fungi or nematodes can be expected
to be particularly sensitive to fluctuations in their immediate
electrochemical environment. Small organisms respond to
changes in their physico-chemical environment with changes in
metabolic activity and behavior (e.g., Fenchel, 2002;Vanreusel
et al., 2010). Disposal of respiratory electrons is essential for
organisms to sustain metabolic activity that drives ecosystem
processes, including respiration and the recycling of organic
matter and nutrients (Cho and Azam, 1988). The availability
of molecules accepting respiratory electrons (i.e., redox
conditions) can hence pose an important constraint on
the metabolic activity of organisms in soils and sediments
(Hayes and Waldbauer, 2006).
While many studies have improved our understanding
of processes governing the Earth’s subsurface electrochemical
environment, many observed variations remain difficult to
reconcile with known drivers of electrochemical heterogeneity.
Here, we briefly synthesize our understanding of drivers of
Earth subsurface electrochemical variability, and present a
novel conceptual foundation relating variations in atmospheric
electricity (AE) to variations in the Earth’s electrochemical
environment and to consequences for the microorganisms living
therein. We present evidence supporting the proposed linkages
and identify challenges for future research.
DRIVERS OF SPATIO-TEMPORAL
VARIABILITY IN EARTH’S SUBSURFACE
ELECTROCHEMISTRY
Small-scale variation in the electrochemical properties of
sediments and soils are mainly controlled by biotic influences.
For instance, locomotive activity of invertebrates that rework
soils and sediments (bioturbation) is a well-known driver
of micro to millimeter-scale redox conditions in both soils
and sediments (Tokida et al., 2007;Hunting et al., 2012).
Bacterial metabolic activity, in particular, is considered to be
mainly controlled by this small-scale variation (Newman and
Banfield, 2002). Redox fluctuations are likely an important
selective pressure on microbes with repercussions for community
composition and activity (Pett-Ridge and Firestone, 2005), for
instance by selecting for metabolically more flexible bacterial
taxa (DeAngelis et al., 2010). In turn, bacteria can secrete
redox-active exudates (e.g., flavins) to maintain favorable redox
conditions (Hunting and Kampfraath, 2013;Markelova et al.,
2018), or can use long-distance (>1 cm) electron transfer to
connect spatially separate bio-electrochemical processes (Nielsen
et al., 2010;Pfeffer et al., 2012). Photosynthesis also promotes
fluctuations in redox-conditions by introducing oxygen into
the upper layers of soils and sediment (Battin et al., 2003;
Laursen and Seitzinger, 2004), resulting in a net diurnal
increase of oxygen concentrations and a net nocturnal decrease
caused by respiration.
While small-scale variations are mainly driven by biological
processes (Masscheleyn et al., 1991;Hayes and Waldbauer,
2006), diel and seasonal fluctuations of concentrations for
many chemical species relevant to microbial processes (e.g.,
denitrification and methanogenesis) are also often linked over
large distances (Lee, 1977;Laursen and Seitzinger, 2004;Allen
et al., 2007;Spencer et al., 2007;Rusjan and Mikoš, 2010;
Bass et al., 2013). The occurrence of large-scale temporal
fluctuations in a wide variety of ecosystems suggests large-
scale abiotic processes are also relevant to soil, sediment and
water electrochemical properties (Scholefield et al., 2005). Indeed,
various abiotic drivers of spatial linkages and synchronized
temporal variability in subsurface chemical concentrations and
microbial activity have been identified. They include solar
activity, groundwater flow, atmospheric pressure, lunisolar and
tidal cycles, and gradients of the chemical potential of charge
carriers (reviewed in Lanzerotti and Gregori, 1986;Tokida et al.,
2007). In inland waters and terrestrial soils, charge separation in
clay or other minerals, contaminants and ground-water flow have
also been shown to influence the electrochemical environment
(e.g., Revil and Jardani, 2013).
Despite the breadth of understanding of processes governing
the Earth’s subsurface electrochemical environment and the
consequences for organisms, the known drivers fail to explain
all observed electrochemical variations. This is especially true for
variations in the deeper layers (up to meters) of Earth’s surface
(Vorenhout et al., 2011). For instance, while photosynthesis can
be responsible for diel variation of redox-conditions in biofilms
and surficial (<1 cm) soil and sediment layers (Battin et al.,
2003;Laursen and Seitzinger, 2004), it unlikely affects deeper
environments and associated organisms, since oxygen diffusion
is slow and consumption by heterotrophs is fast (Laursen
and Seitzinger, 2004). Here, we propose a new perspective
based on the idea that variation in AE is an additional
factor underlying cyclic variation in the electrochemistry and
associated microbial communities and activities in the Earth’s
subsurface environment.
CONCEPTUAL FOUNDATION OF
RELATIONSHIPS BETWEEN
ATMOSPHERIC ELECTRICITY, EARTH’S
SUBSURFACE ELECTROCHEMISTRY
AND MICROBIAL COMMUNITIES
Electrical properties of the near-surface atmosphere (e.g., ion
concentrations and the atmospheric potential gradient) vary
on daily and seasonal times scales (Israelsson and Tammet,
2001;Harrison, 2004). An atmospheric electric field is present
even in fair-weather regions as a consequence of global electric
current flows driven by thunderstorm regions (e.g., Rycroft et al.,
2000;Haldoupis et al., 2017). Locally, environmental conditions,
radioactive decay of radon, charges of aerosols, and atmospheric
pollution may further contribute to variation in atmospheric
electric conditions (Matthews et al., 2019). The combination
of global and local variations in AE leads to variations over
various spatial and temporal scales, with diel fluctuations being
particularly important (Israelsson and Tammet, 2001). The
universal diel pattern in vertical current and potential gradient
is dominated by a minimum at around 04 Universal Time
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FIGURE 1 | Conceptual diagram depicting the proposed link between atmospheric electricity (AE), Earth surface electrochemistry and microbial processes. Electrical
variations of cations (+) in the atmosphere are governed by a variety of factors, including cosmic rays, variation in the ionosphere, radioactive decay of radon and
other elements, global thunderstorm activity and solar radiation. Since the Earth surface is negatively charged (–), the resulting vertical current forces ions to move
within soils and sediments. This includes the major ions required for microbial metabolic activities in anoxic environments. These changes in resource supply caused
by electrical variation in the atmosphere can thus influence the spatial and temporal patterns of biogeochemical processes. The major terminal electron acceptors
used in anoxic microbial metabolism can be either anions or cations (indicated by a – or + sign, respectively). Anions such as nitrate (NO3−) and sulfate (SO42−)
move toward the atmosphere, whereas cations such as iron (Fe2+) and manganese (Mn2+) move deeper into the soil or sediment. Free electrons produced by
microbial metabolism at the Earth surface could also potentially be directed toward the atmosphere, as indicated by the curved dotted arrow.
(UT) and a maximum at around 19 UT. This universal pattern
is clearest in clean maritime air where aerosol pollution and
other local sources of variation (e.g., diel fluctuations in radon
concentration) are minimized. In contrast, over land diel patterns
are more influenced by local variations in AE (Israelsson and
Tammet, 2001;Harrison, 2004).
Electric currents rely on movement of (small) ions in the
atmospheric electric field, and typically range between 0.5 and
3.0 pA m−2at the Earth surface interface, where the currents
subsequently enter the Earth surface as part of the global
electric circuit (Rycroft et al., 2008;Harrison, 2013). Other
geophysical processes (e.g., groundwater flow) contribute to
influencing the electrical properties of the Earth subsurface
(Lanzerotti and Gregori, 1986;Wada and Umegaki, 2001;Revil
et al., 2010). In soils, water bodies, and their sediments, currents
induced by variations in AE likely influence the release of
respiratory electrons and movement of ions, thereby critically
affecting redox conditions with repercussions particularly for
microorganisms. For instance, variations in AE could induce
the vertical movement of charged terminal electron acceptors
that are essential for microbial respiration (see Figure 1 for
a conceptual diagram). Terminal electron acceptors relevant
to microorganisms (e.g., NO3−, Mn43+, and SO42−) differ in
size and charge, suggesting that they move at different speeds
within Earth subsurface environments. Moreover, ion movement
is influenced by the electrical conductivity of water, soils and
sediments. Surface soil layers, for instance, typically have a
conductivity of 0.1–2.0 dS/m (Rhoades and Corwin, 1981), which
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is low compared to seawater, for instance (∼4 S/m; e.g.,
Al-Shamma’a et al., 2004), and may impede long-distance (Revil
et al., 2010) but not short-distance (µm – mm – cm) ion
movement (Wada and Umegaki, 2001;Mann et al., 2005). Such
variation in redox properties of soils and sediments driven by
AE likely affects the ability of microbes to dispose of their
respiratory electrons (Figure 1). To date, the consequences
of variation in AE on the electrochemical properties of
subsurface ecosystems and the organisms living therein remains
entirely unexplored.
FIGURE 2 | Effect of elevated levels of atmospheric cations on redox conditions, bacterial respiratory activity and H2S concentrations (sulfate reduction) in sediments
of aquatic microcosms. (A) Redox potential, Eh, was measured at 1 and 6 cm sediment depth in response to manipulated atmospheric cation concentrations.
(B) Bacterial respiratory activity, measured as electron transport system (ETS) activity (expressed as relative absorption at 490 nm), was significantly lower in control
microcosms than in microcosms in which the atmosphere was ionized for 24 h (t-test, p= 0.002, n= 6). (C) Changes in bacterial H2S concentration at different
sediment depths in response to ionization of the overlying atmosphere (left panel), suggesting a shift in H2S production toward the surface as a result of upward
SO42−movement (conceptually depicted in right panel). Shaded areas and (+) indicate periods of experimental ionization. A single time-series measurements is
presented for clarity and considered representative of replicate (n= 12) runs.
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EVIDENCE FOR LINKAGES BETWEEN
ATMOSPHERIC ELECTRICITY,
SUBSURFACE ELECTROCHEMISTRY
AND MICROBIAL METABOLIC ACTIVITY
Laboratory Experiments
We conducted several laboratory experiments to explore effects
of variation in AE on sediment redox conditions and bacterial
metabolism (for a description of the experimental approach see
Supplementary Material S1). We found that sediment redox
potential (Eh) in aquatic microcosms evolved independently
of sediment pH (max. change ±0.1 units) or oxygen
concentration (max. change ±1% saturation), when exposing
them to experimentally manipulated levels of atmospheric ion
concentrations. In contrast, Ehgradually increased at different
sediment depths, starting immediately when ionization began,
then declined and quickly stabilized when disrupting ionization
(Figure 2A). Control microcosms in which the overlying
atmosphere was not ionized soon reached a redox equilibrium
that remained constant throughout the experiment (data not
shown). No effects on Ehin the sediment were found after
exposing the microcosms to radiation [UV A, B, and C as
well as photosynthetically active radiation (PAR) and infrared;
data not shown]. Taken together, our empirical data shows
that fluctuations of Ehin the microcosm sediment were
independent of solar radiation but were strongly influenced by
the manipulated shifts in ion concentrations in the overlying
atmosphere. These findings provide clear evidence that variations
in AE have potential to influence geochemical and microbial
processes via alterations of Eh.
We then tested the response of bacterial communities
in sediments of microcosms to fluctuations in Ehinduced
by variations in AE laboratory conditions by increasing
concentrations of ions in the overlaying atmosphere. We
measured the respiration of the bacterial community as ETS
activity in the upper sediment layer (<1 cm) after 1 day of
exposure to atmospheric ionization and observed a two-fold
increase (t-test, p<0.05) compared to control microcosms
(Figure 2B). However, since multiple bacterial processes
can contribute to ETS activity, the cause of the increase
remains uncertain.
To examine the issue further, we experimentally exposed
aquatic microcosms to increased concentrations of ions in
the overlaying atmosphere and assessed H2S concentrations
in response to atmospheric ionization. We chose H2S
concentration as the most informative response variable,
since it results directly from SO4−reduction. Moreover,
since H2S does not carry a charge, any changes in H2S
due to variation in AE can only result from changes in
SO4−reduction. We observed a gradual increase in H2S
concentrations at 4 mm below the sediment surface, whereas
H2S concentrations decreased at 6 mm below the sediment
surface. The response in H2S concentrations after the start of
ionization was slightly delayed (Figure 2C). These findings
suggest that the depth of maximum SO42−concentrations
shifted toward the sediment surface in response to ionization
where the microbial community quickly responded by reducing
SO42−to H2S.
FIGURE 3 | Fair weather diel fluctuations in sediment redox potential and AE.
(A) Redox potential (Eh) measured at 10 cm depth of a natural pristine
sediment as a single run over 3 days in Lake Cadagno, an alpine lake in
Switzerland, in October 2017. (B) The universal periodicity in atmospheric
electrical properties (expressed as potential gradient, PG, between
atmosphere and ground), which is visible around the globe during fair weather
conditions (Harrison, 2013). All data is plotted against universal time, UT, and
represent single time-series measurements. Peaks at 19 UT indicate that
fluctuations in redox conditions are governed by global patterns in AE.
FIGURE 4 | Coherence of temporal changes in net atmospheric cation
concentrations and sediment redox conditions. Redox potential (Eh) was
measured on 24 October 2013 at different depths (1, 2, 3, and 6 cm) in sandy
sediment of a ditch in Netherlands. Data of this single run is plotted against
local time (GMT +2).
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FIGURE 5 | Fair weather diel rhythms in sediment redox potential outdoor mesocosms experiencing different levels of bioturbation. Contour plots show depth
profiles (0–9 mm) redox potential (Eh) over 4 days in three different mesocosms. Mesocosms contained different combinations of invertebrates known to rework
surface sediment to various degrees: (A) no bioturbation: invertebrates lacking; (B) low level of bioturbation: Tubifex spp. and Asellus aquaticus; and (C) high level of
bioturbation: Gammarus pulex,Asellus aquaticus,Chironomus riparius,Tubifex spp., and Lumbriculus variegatus.
Field Observations
To evaluate whether the links between AE and subsurface redox
variations observed in microcosm experiments apply in realistic
settings, we measured Ehin (1) an outdoor mesocosms facility
containing no or different combinations of invertebrates causing
bioturbation of surface sediments; (2) freshwater sediments at
two distinct sites, and (3) soils at geographically distinct locations
(see Supplementary Material S1 for details). In the shallow
littoral zone of pristine Lake Cadagno in the Swiss Alps, we
observed diel fluctuations in Ehfollowing the universal cycle in
atmospheric potential gradient, with peaks occurring at around
19 UT (Figure 3). In contrast, in a ditch experiencing urban
pressure in Netherlands, the diel fluctuation was dominated
by local influences, with a peak occurring at around 2–4 pm
local time (Figure 4). However, the number of cations in the
ground-level atmosphere also appeared to covary with sediment
Eh(Figure 4).
Diel fluctuations in Ehin response to local variation in
AE were also observed in sediments of freshwater outdoor
mesocosms in Netherlands (Figure 5 and Supplementary
Figure S1). Here, diel patterns were visible even in the presence
of invertebrates reworking the upper sediment layers, and were
more pronounced during fair-weather conditions than on cloudy
days (Supplementary Figure S1). These diel rhythms were not
observed to covary with other tested meteorological variables
such as solar radiation, temperature and air pressure (data not
shown). This finding indicates that the postulated link between
AE and sediment redox potential persists also when major
hydrological and geophysical processes (e.g., groundwater flow)
are excluded. This supports our hypothesis that a direct link exists
between subsurface Ehand AE. Interestingly, natural freezing of
the top water layer in the mesocosms served as an unplanned
experimental control, since the co variation between subsurface
Ehand AE disappeared, probably as a consequence of poor
conductive properties of ice (data not shown). Finally, Ehin
soils at three distant sites also followed diel patterns in AE
whose influence extended relatively deep into the soil (typically
50–100 cm; Figure 6).
These outdoor measurements suggest that variation in
subsurface redox potential can follow both the universal diel cycle
in the atmospheric potential gradient (Figure 6) and local sources
of variation affecting atmospheric cation concentrations at
ground level (<1 m). Together with our laboratory results, these
field observations reveal that both global and local variations in
AE influence redox conditions and microbial processes in soils
and sediments, in which strong local influences on redox patterns
can dominate in some locations.
IMPLICATIONS AND PERSPECTIVES
The findings from our laboratory experiments and field
observations support the hypothesis that variation in AE can
influence Ehin different soil and sediment matrices with
consequences for microbial communities in these environments.
The significance of this phenomenon in natural settings remains
unclear, however, because persisting knowledge gaps impede a
conclusive understanding of the causal relationships between AE
and Earth’s electrical environment. Challenges for future research
range from elucidating the relevant scales of the physical and
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FIGURE 6 | Fair weather diel rhythms in soil redox potential and AE. Redox potential (Eh) measured in natural soils: (A) at 50 cm depth in Netherlands (52.2◦N,
4.5◦E; GMT + 2) between 1 and 3 May 2011, (B) at 50 cm depth in Netherlands (52.4◦N, 6.1◦E) between 1 and 3 July 2011, and (C) at 1 m depth in Bangladesh
(23.8◦N, 90.6◦E; GMT + 6) between 27 and 30 March 2010. Lines represent measurements of single time series. (D) The universal periodicity in atmospheric
electrical properties (expressed as potential gradient, PG, between atmosphere and ground) that is visible around the globe during fair weather conditions (Harrison,
2013). All data is plotted against, UT. Peaks at 19 UT (visible in panels B,C) indicate that fluctuations in redox conditions are governed by global variations in AE
(B,C), while peaks at 16 UT (visible in panel A) indicate that fluctuations in redox conditions are primarily governed by local variation in AE (A).
chemical linkages to how these links directly or indirectly govern
distinct groups of organisms.
How specific chemical species and organisms respond to
changes in AE likely depends on the relative magnitude of a
combination of various physical sources of variations. These
include solar activity, groundwater flow, gradients of the chemical
potential of charge carriers (reviewed in Lanzerotti and Gregori,
1986;Revil and Jardani, 2013), as well as electrochemical soil
and sediment properties, including electrical resistance and the
size and charge of terminal electron acceptors. Unraveling the
absolute and relative roles of regional and global-scale drivers of
variation in AE (Märcz and Harrison, 2003;Harrison, 2004) and
redox potentials in water, sediments and soils would thus be a
promising, though challenging research field. Earth subsurface
electrochemistry varies in depth, and hence future work needs
to assess to which extent variations in AE can translate to
synchronized responses in Earth subsurface electrochemistry in
relation to the conditions at different soil and sediment depths
(e.g., moisture, conductivity, Eh). Likewise, it is necessary to
partition the role of AE in relation to other major drivers of
Earth subsurface electrochemistry. This requires coordinated
field experiments over a wide range of geographical locations to
assess the significance on a global scale and the importance of
local influences in superimposing universal rhythms.
The coupling between AE and subsurface electrochemistry
observed in our field and laboratory studies also suggests
that microorganisms in these environments are vulnerable to
anthropogenic influences affecting variation in AE. In particular,
anthropogenic pollution by smoke, sulfur dioxide and aerosols
can affect AE (Retalis et al., 1991;Sheftel et al., 1994;
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Kamra and Deshpande, 1995). Our results suggest that such
pollutants could have strong, though currently unknown, indirect
effects on subsurface microorganisms and processes by affecting
temporal patterns of AE. Furthermore, electrical pollution by
high-voltage power lines (mostly operated with alternating
currents) is a common local factor affecting variations in AE
(Maruvada, 2012). The resulting static electric fields have been
observed to trigger responses in a wide array of organisms,
particularly behavioral responses in invertebrates (Petri et al.,
2017;Schmiedchen et al., 2018). However, these studies were
limited to flying insects and invertebrates on top of soils, and
hence potential impacts of static electric fields on subsurface
microorganisms and invertebrates went unnoticed. Nonetheless,
power lines could influence soil and sediment communities
and processes in at least two ways: First, shedding of ions
provides a secondary source of pollution that may change
direct current and ion transport in local environments with the
consequences on microbial communities and processes described
above. Second, strong variation in electric fields affect organisms
using them for orientation (i.e., galvanotaxis or electrotaxis).
Such behavioral responses have been observed for bacteria and
invertebrates such as nematodes (Bespalov et al., 1996;Chrisman
et al., 2016) and might further complicate the electrochemical
environment in soils and sediments, which many organisms can
alter (Traunspurger et al., 1997;Weerman et al., 2011;Hunting
et al., 2013, 2015;Hunting and Kampfraath, 2013). Effects of local
electrical pollution are readily amenable to tests in laboratory
conditions by manipulating electric variables, but they can also
be validated in natural settings (e.g., under power lines).
CONCLUSION
Our results from experiments and field observations suggest
that variation in AE can influence Earth’s subsurface chemistry
and the microorganisms in subsurface environments. We have
provided proof of evidence that variations in AE can cascade
down to changes in sediment redox conditions with implications
for microbial electron transport activities and biogeochemical
processes such as SO4−reduction. These insights widen our
conceptual understanding of processes in water bodies, soils and
sediments, and their overlooked links to AE. The coupling of AE
and subsurface electrochemistry is likely relevant to a wide range
of organisms, in particular those with electrotactic behavior such
as many microbial and nematode species. The proposed concept
that AE could serve as a sinus node that sets the pace of Earth’s
biogeochemical heartbeat also presents many unknowns that call
for pursuing diverse research avenues in the future.
AUTHOR CONTRIBUTIONS
EH conceived, designed, and coordinated the study. RH and
AK were involved in the initial conception. EH, AB, MV, and
CC collected the field data. HvdG and PvB participated in the
design of the study. HvdG, EH, and AK participated in the design
of the conceptual figure. EH performed the experiments and
statistical analyses. EH, RH, and MG drafted the manuscript.
WA, PvB, AB, and HvdG contributed significantly to the earlier
drafts. All authors contributed to improve the earlier drafts
of the manuscript.
ACKNOWLEDGMENTS
We thank Andrew Boulton, Martina Vijver, and Jack Middelburg
for constructive comments on earlier drafts of the manuscript,
Frank Hammecher, Gerard Muyzer, and Catarina Cucio for
useful discussions and assistance, and Hans Agema and Tijs van
Roon for technical support. We are grateful to Dré Kampfraath
and Frans Schupp for the graphical design of the conceptual
diagram (Figure 1). We acknowledge the facilities provided by
the Centro Biologia Alpina, Piora. Part of this work developed by
participating in the COST Action 15211 Atmospheric Electricity
Network: coupling with the Earth System, climate and biological
systems, supported by the European Union COST (European
Cooperation in Science and Technology) Program.
SUPPLEMENTARY MATERIAL
The Supplementary Material for this article can be found
online at: https://www.frontiersin.org/articles/10.3389/fphys.
2019.00378/full#supplementary-material
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Conflict of Interest Statement: The authors declare that the research was
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Kampfraath, Vorenhout, Admiraal, Cusell and Gessner. This is an open-access article
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