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MARK BRINSON REVIEW
Amir Neori
1
&Moshe Agami
2
Received: 19 May 2015 /Accepted: 25 February 2016 /Published online: 17 March 2016
#Society of Wetland Scientists 2016
Abstract Anoxia and harmful metabolites are two of sev-
eral particularities that characterize wetland soils and
make their study so fascinating. Unique physiological
and anatomical adaptations in roots of wetland plants al-
low them to exploit the light, water and nutrients available
in the wetland. The adapted roots are surrounded by a
rhizosphere, which attracts by its water, oxygen, nutrients
and physical protection a myriad of wetland-specialized
organisms. These organisms, which include viruses, bac-
teria and archaea (such as N-fixers, nitrifiers and
methanotrophs), fungi (such as mycorrhizal fungi), proto-
zoa and animals, determine the ecological functioning of
the vegetated wetland through their interactions with the
roots, with each other and with their inanimate environ-
ment. Several of these interactions, especially the globally
significant immobilization of carbon and emission of
greenhouse gases, are unique to wetlands. The present
review highlights the main issues and gaps in our under-
standing of the contribution of rhizosphere biota to the
ecological functioning of the widespread and globally im-
portant vegetated wetlands. Multi-disciplinary research
teams that use modern technologies and approaches could
help close these gaps.
Keywords Anaerobic .Anoxic .Archaea .Bacteria .
Biogeochemical processes .Flooded soils .Fungi .
Interactions .Invertebrates .Mycorrhizal fungi .Nematodes .
Protozoa .Roots .Viruses
Introduction
Wetland ecosystems encompass all forms of vegetated
flooded soils, such as swamps, marshes, salt marshes, bogs,
fens, mires, moors and peatlands (Mitsch and Gosselink
2000). Natural wetlands and paddy rice cover merely 6 % of
the global vegetated land area, yet they contribute over 10 %
of the global terrestrial primary production, over a third of the
total organic carbon storage in soils and a third of the global
methane (CH
4
) emissions (Aselmann and Crutzen 1989;
Fourqurean et al. 2012; Running 2012;Xuetal.2013;
Weston et al. 2014). The value estimates of the ecosystem
functions and services provided per unit area are 10–100 fold
higher in wetlands then in dryland and ocean ecosystems;
consequently, wetlands provide about a quarter of the global
value of ecosystem services (Costanza et al. 2014).
Understanding the functioning of these important ecosystems
is, therefore, vital.
Plants and the soil biota account for much of the value of the
wetlands. Plants photosynthesize by their aboveground organs,
while their roots and their rhizospheres drive the belowground
productivity of the heterotrophic soil biota (Bonkowski et al.
2009). Anoxia and harmful metabolites (e.g., hydrogen sulfide,
organic acids, ammonia and CO
2
) make the wetland soil hostile
to plants and other organisms (for further information, see
Kowalchuk et al. 1998; Mitsch and Gosselink 2000;
Kinsman‐Costello et al. 2015). Wetland plants, which are of
the earliest of land plants, have adapted to these conditions
(van Dam 2009; Maberly 2014).
*Amir Neori
neori@ocean.org.il; aneori@gmail.com
1
National Center for Mariculture, Israel Oceanographic and
Limnological Research, POB 1212, Eilat 88112, Israel
2
Department of Molecular Biology and Ecology of Plants, The
George S. Wise Faculty of Life Sciences, Tel Aviv University,
6997801 Tel Aviv, Israel
Wetlands (2017) 37:615–633
DOI 10.1007/s13157-016-0757-4
The Functioning of Rhizosphere Biota in Wetlands
aReview–
The plants interact with the soil through their rhizosphere,
which is a loosely–defined region of soil that surrounds the
roots and is impacted by them (Armstrong 1978; Curl and
Truelove 1986). Wetland rhizospheres are created by the
roots’aeration and detoxification of the anoxic bulk soil; they
are essentially Boxic island^habitats, or niches, which expand
greatly the diversity of the wetland’s heterotrophic biota
(Crawford 1987;Blom1990; Gopal and Masing 1990;
Bodelier 2003;JacksonandJackson2008). The rhizosphere
soil is one (the other two are oxic surface soil and anoxic bulk
soil) of the three main distinct functional components of the
vegetated wetland (Liesack et al. 2000). The dimensions of the
rhizosphere are transient. They depend on the one hand on the
plant’s metabolism (especially the rate of photosynthesis), as it
is expressed by root’s emission of oxygen and rhizodeposits
(root exudates, lysates, mucilage, dead cell material and bio-
active and gaseous compounds) that impact the nearby biota
(e.g., Neori et al. 2000; Bonkowski et al. 2009; Ellouze et al.
2011; van der Valk 2012;Stirling2014; Rakshit et al. 2015).
On the other hand, these dimensions also depend on the me-
tabolism of the biota, in addition to the soil and the environ-
mental conditions (Ravit et al. 2006; Nikolausz et al. 2008;
Stout and Nüsslein 2010).
The heterotrophic biota of the wetland consists of numer-
ous organisms that live in close proximity, ranging from vi-
ruses, bacteria and fungi to larger organisms. They perform a
myriad of functions and are responsible for the processes that
characterize wetlands, among them the globally-important
generation of greenhouse gases, especially CO
2
, methane-
CH
4
and nitrous oxide-N
2
O(AgamiandWaisel1986;
Gärdenäs et al. 2011). Understanding the functioning of wet-
lands necessitates, therefore, an understanding of their hetero-
trophic biota. Heterotrophic organisms that live in the rhizo-
sphere of wetland plants rather than in the bulk wetland soil
are rewarded by oxygen, food, bioactive protection, substrate
and shelter, yet they risk predation and disease by other or-
ganisms and inhibition by bioactive chemicals (Makulova
1970;Kuoetal.1981; Hendrarto and Dickinson 1984;
Wetzel 1992; Heckman 1994; Kowalchuk et al. 1998;
Wetzel 2000; Feeney et al. 2006; Vymazal 2011; Bardgett
and van der Putten 2014;Kinsman‐Costello et al. 2015;
Nielsen and Risgaard-Petersen 2015). The root tissue itself
attracts a myriad of pathogens as well (Strandberg 1987;
Papadimitriou et al. 2010). The biota in the rhizosphere of
the wetland plant is, therefore, not only unique but also much
denser than in the bulk of the flooded soil (Gunnison and
Barko 1989; Hairiah et al. 2001;Devereux2005; Vladár et
al. 2008; García-Martínez et al. 2009; Hinsinger et al. 2009).
Wet surface interfaces, especially rhizoplanes (root sur-
faces), are often the largest and dominant surfaces of the wet-
land, and where the main microbial processes take place
(Smith et al. 1979; Francour and Semroud 1992;Duarteet
al. 2005;JacksonandJackson2008). The rhizoplane is the
focal plane of perpendicular gradients in the concentration of
oxygen, toxins, nutrients and redox potential; gradients are
crucial to the functioning of wetland ecosystems because
many organisms depend on them (Andersen and Hansen
1982; Bottomley and Bayly 1984; Smith et al. 1984;
Andersen and Kristensen 1988; Liesack et al. 2000; Wang et
al. 2012). Gradients intensify the diversity and the activity of
the biota in wetland soils, compared to dry soils (Wetzel 1992;
Liesack et al. 2000; Neori et al. 2000;Lamersetal.2012;Wu
et al. 2013).
The complementary processes by the plants and their rhi-
zosphere’s organisms precipitate a resilience to pollutants and
contribute to the bioremediative capacity of vegetated wet-
lands (Wenzel 2009). Surprisingly, however, fewer studies
have examined the functioning of wetlands belowground,
compared to wetlands aboveground. The available relevant
studies, which often address bioremediation, have often treat-
ed wetlands belowground ecosystems as Bblack boxes^and
dodged the complexity of the aforementioned interactions
(Cannicci et al. 2008; Murase and Frenzel 2008; Cherry
2011; Henry and Twilley 2013).
When we first read the literature available on the biota of
wetland rhizospheres, in the early to mid 1990’s, the informa-
tion seemed to us inadequate for the completion of this over-
view. This has now changed, as the last two decades have
produced many multidisciplinary research publications that
describe efforts with improved methodologies directed at un-
derstanding the role of rhizosphere biota in wetland function-
ing. This rise in interest can be exemplified by a comparative
survey of the number of publications that appeared until 1995
and in the last two decades (the columns designated ‘A’and
‘B’, respectively, in Table 1), on topics that seem to us the
most relevant for the present article, i.e., wetlands, rhizo-
spheres and their biota (the ‘subject’column in Table 1).
The number of all the publications that focused separately
on one of the several designated organism groups and wetland
types covered in the present review rose between the two
periods less than twofold (Table 1a). The numbers of publica-
tions that focused on the general terms ‘biota’,‘rhizosphere’
or ‘wetland’, the main issues of the present review, increased
in the second period 2.7, 3.1 and 8.7 fold, respectively (Table
1a). The numbers of publications that focused on ‘wetland’
and on at least one additional designated organism group
(‘bacteria’,‘invertebrate’,‘fungi’,‘virus’or ‘protozoa’)o
r
on ‘rhizosphere’were small initially, but rose during the sec-
ond period by large factors, between 2.7 and 9.8 fold (Table
1b). Similarly, the numbers of publications that focused on
‘rhizosphere’and an additional surveyed biota group were
small initially, but rose during the second period between
2.1 and 7.8 fold (Table 1c). Publications that focused together
on three of the surveyed topics, i.e.,‘wetland’,‘rhizosphere’
and one of the main biota groups (‘bacteria’,‘invertebrates’,
‘fungi’,‘virus’or ‘protozoa’), scored the lowest out of all the
616 Wetlands (2017) 37:615–633
surveyed categories, but showed (except for ‘virus’) the most
dramatic increases during the second period, between 6.3 and
16.4 fold (Table 1d). As an example, the number of publica-
tions that focused together on three subjects - ‘bacteria’and
‘wetland’and ‘rhizosphere’- rose during the second period
7.1 fold (Table 1d); the number of publications that focused on
only two subjects - ‘bacteria’and either ‘wetland’or ‘rhizo-
sphere’- rose during the second period only 2 to 3 fold (Table
1b and c); the number of publications that focused on ‘bacte-
ria’alone was similar in the two periods (Table 1a). The as-
tonishing rise seen between the mid 1990’s and the present in
the publication rate of scientific publications that integrate the
study of an organism group with ‘wetland’and with ‘rhizo-
sphere’reflects, in our opinion, increases in both the scientific
appreciation of the complexity of this ecosystem and the tech-
nical capability for such complex studies.
The present article summarizes critically the published ev-
idence and ideas regarding the populations, activities and
functions of the organisms –microbiota and small fauna - that
are associated specifically with the rhizospheres of wetland
plants. Although larger animals such as insects, molluscs, fish,
birds and mammals also interact with the wetland rhizosphere,
Tabl e 1 Results of a literature
search
a
for publications that
mentioned specific topics with a
relevance to wetland-rhizosphere
biota. Left hand column: the
searched terms; Column-A: the
number of publications up to
1995; Column-B: the number of
publications between 1996 and
September 2015; Right hand
column: the ratio between
columns A and B (B/A ratio).
Section: (a) the publications that
mentioned one topic; (b) the
publications that mentioned
‘wetland’and an additional topic;
(c) the publications that
mentioned ‘rhizosphere’and an
additional topic; (d) the
publications that mentioned
‘wetland’,‘rhizosphere’and an
additional topic
Subject Number of publications
A:Up to 1995 B:From 1996 B/Aratio
(a)
Bacteria 1,310,000 1,190,000 0.9
Salt-marsh 17,100 18,000 1.1
Marsh 617,000 703,000 1.1
Virus 433,000 504,000 1.2
Bog 72,000 85,500 1.2
Protozoa 67,300 85,100 1.3
Fungi 869,000 1,110,000 1.3
Plant 428,000 582,000 1.4
Swamp 75,600 109,000 1.4
Invertebrates 107,000 195,000 1.8
Peat land 42,200 81,500 1.9
Biota 50,000 130,000 2.7
Rhizosphere 24,700 75,700 3.1
Wetland 48,100 420,000 8.7
(b)
Wetland Bacteria 7910 21,700 2.7
Wetland Invertebrates 7620 22,200 2.9
Wetland Fungi 3670 19,000 5.2
Wetland Rhizosphere 2810 15,300 5.4
Wetland Virus 2270 15,900 7.0
Wetland Protozoa 1480 14,500 9.8
(c)
Rhizosphere Bacteria 14,100 29,300 2.1
Rhizosphere Fungi 12,000 27,200 2.3
Rhizosphere Virus 2490 11,300 4.5
Rhizosphere Protozoa 1190 7900 6.6
Rhizosphere Invertebrates 1290 10,100 7.8
(d)
Wetland Rhizosphere Virus 1170 2260 1.9
Wetland Rhizosphere Fungi 1560 9770 6.3
Wetland Rhizosphere Bacteria 2130 15,100 7.1
Wetland Rhizosphere Invertebrates 202 2260 11.2
Wetland Rhizosphere Protozoa 102 1670 16.4
a
Google Scholar (Breferences^and Bpatents^unchecked), September 2015.
Wetlands (2017) 37:615–633 617
they fall outside the scope of this article. In concurrence with
Andrén et al. (2008), this review has purposely included older
and grey literature that may be unavailable or practically
forgotten.
Organisms and Their Functions
General
Organisms that carry out the biogeochemistry of flooded soils,
especially methanogens, denitrifiers, sulfate reducers, fermen-
ters and acetogens (Gutknecht et al. 2006;Lamersetal.2012;
Bodelier and Dedysh 2013), existed long before the emer-
gence of plants and animals. The plants that populated flooded
soils at first were probably those that managed to live with the
prevailing conditions and resident biota. Much of the biota
that lives in wetland soils today, however, has seemingly
evolved to utilize the patches of rhizosphere niches within
the otherwise inhospitable flooded soils. Evidently, the advan-
tages in the regimes of water, gases, pH and nutrient content in
rhizospheres compared with the bulk soil promote the in-
creased diversity, biomass and activity in the biota of today’s
wetland rhizosphere soils (Agami and Waisel 1986;Tianetal.
2013;Liaoetal.2015).
The dearth of studies that integrate wetland processes, or-
ganisms and functions probably stems from the tendency of
the early wetland specialist scientists to pay attention to an
individual organism, a component or a process of the wetland,
based on their personal competence and interest (Gaskins et al.
1985; van Groenigen et al. 2014; Nielsen and Risgaard-
Petersen 2015). Fortunately, more complex multi-
disciplinary studies, especially with microorganism, have ap-
peared in the last two decades (Table 1). This development
benefitted tremendously from the advances made in culture-
independent molecular technologies (Stirling 2014). However,
studies of multiple-organism interactions and processes are still
scarce, and therefore the role that various organisms play in the
biogeochemistry of the wetland rhizosphere remains relatively
obscure (Osenga and Coull 1983;Orthetal.1984; Hackney
1987;delaCruzetal.1989; Gopal and Masing1990; Boström
et al. 2006; Gutknecht et al. 2006; van Dam 2009; Leduc and
Probert 2011;Ohtakaetal.2011;Vymazal2011; Basiliko et al.
2012; Churchland et al. 2012; Fenchel et al. 2012;Ohtakaetal.
2014; Liao et al. 2015).
Viruses
Viruses influence profoundly aquatic communities and bio-
geochemical cycles (Fuhrman 1999;Suttle2005; Raven
2006; Jackson and Jackson 2008; Middelboe et al. 2008;
Jacquet et al. 2010). Viral infection generates exchanges of
genetic information between organisms and progeny viruses,
thereby driving the evolution of both the host and the viral
assemblages (Suttle 2005). Viral infections of cells that par-
ticipate in the microbial loop - the cycling of organic matter
and nutrients between the dissolved phase and small cells,
without it flowing into the grazing food chain (Jackson and
Jackson 2008) - decimate essential organisms and short-circuit
food webs. In this way viruses modify and redirect flows of
energy, organic matter and nutrients (Li et al. 2013).
Aquatic viruses and their functions have been studied in
wetlands soils and water more than in wetland rhizospheres
(Williamson et al. 2005;Kimuraetal.2008). Virus density in
marine sediments is several orders of magnitude higher than it
is in marine water (Williamson et al. 2005;Danovaroetal.
2011). The viral impact on the nutrient pathways in wetland
soils, particularly in rhizospheres where the viruses and their
target organisms are numerous and intermingled, should
therefore theoretically be severe. However, this remains large-
ly unexplored (e.g.,Lietal.2013).
The abundance of soil viruses, many of which might be
phages, depends on bacterial abundance and activity
(Weinbauer and Rassoulzadegan 2004). The viral infection
controls bacterial populations and mediates gene transfer in
soils (Ashelford et al. 2003). The abundance of bacteria and
viruses in the rhizosphere of terrestrial plants peaks during
rapid plant growth, a dynamic situation that is likely to occur
in wetlands as well (Jackson and Jackson 2008).
Phytopathogenic viruses also kill root cells and beneficial rhi-
zosphere organisms (Ahmad 1990). Plant roots and rhizo-
sphere microbes reciprocate, by protecting themselves with
antiviral agents (Neori et al. 2000; Nagarajkumar et al.
2004). Much of the relevant knowledge regarding wetland
viruses is related to viral pathogens of rice (like in
Nagarajkumar et al. 2004). There are also studies on the fate
of pathogenic viruses that drift through wetlands in the waste-
water, but only few publications describe the ‘resident’soil
viruses that function within this ecosystem (Vymazal 2005;
Jacquet et al. 2010; Verbyla and Mihelcic 2015). Viruses af-
fect the resident bacterial populations in vegetated soils under
marine aquaculture facilities (Weinbauer and Rassoulzadegan
2004; Luna et al. 2013). Fish waste stimulates prokaryotic
metabolism and viral infection, reduces bacterial diversity,
alters microbial assemblage composition and affects the activ-
ities of microbes and viruses in the sediments within seagrass
(Posidonia oceanica) meadows; the interactions between vi-
ruses and bacteria are influenced by the level of vegetation of
the sediments (Weinbauer and Rassoulzadegan 2004;Lunaet
al. 2013), suggesting an involvement of the roots.
In summary, the rhizosphere of aquatic macrophytes,
thanks to its unique conditions and biota, might be a signifi-
cant and yet unrecognized reservoir of wetlands-specific vi-
ruses and viral impacts (Jackson and Jackson 2008; Wang
et al. 2012). Their role in the microbial loop and as pathogens
can make viruses crucial to the functioning of vegetated
618 Wetlands (2017) 37:615–633
wetlands (Williamson et al. 2005). This relatively recent real-
ization has been profoundly changing the perception of bio-
geochemistry in the wetland ecosystem (Moebus 1987;Paul
1993; Middelboe et al. 2008).
Bacteria and Archaea- General
The rhizosphere of wetland plants hosts thriving populations
of bacteria and archaea that differ, qualitatively and quantita-
tively, from those found in the bulk soil; they are usually
enriched with species involved with nutrient transformations
(Stout 1971;Úlehlová1976; Blotnick et al. 1980;Dickinson
1983;CurlandTruelove1986;GunnisonandBarko1989;
Sidorenko 1989; Marschner et al. 2004;Herrmannetal.
2008; García-Martínez et al. 2009; Vymazal 2011;Xuetal.
2013). Other species infect pathologically roots and other rhi-
zosphere biota (Ahmad 1990; Lee et al. 1990;Nagarajkumar
et al. 2004; Ehrenfeld et al. 2005; Nelson and Karp 2013).
Bacteria and archaea are often attracted chemotactically
by root exudates and metabolites (Agami and Waisel 1986;
Wang et al. 2015). The main biogeochemical processes that
characterize wetlands are performed by bacteria and ar-
chaea (Brix 1987; recently reviewed by Faulwetter et al.
2009;Oyewole2012;ChandraandKumar2015). The pro-
cesses that have earned the most interest with respect to the
global impact of wetlands and their function in wastewater
treatment have been those that involve organic matter res-
piration, and transformations of the various forms of nitro-
gen (N), phosphorus (P), sulfur (S), metals (especially Fe,
Mg and Se) (Gunnison and Barko 1988a; Laanbroek 1990;
Azaizeh et al. 2003; Vymazal 2007;Herrmannetal.2008;
Stout and Nüsslein 2010; Shpigel et al. 2013), and methane
(Faußer et al. 2012;Görresetal.2013). The production of
methane and nitrous oxide makes wetlands a ‘big’player in
the global greenhouse gases’balance (Schipper and Reddy
1996; Segers 1998; Kumaraswamy et al. 2000;Bridgham
et al. 2013). Microbial production and consumption in soils
of methane (methanogens and methanotrophs) and nitrous
oxide (nitrifiers and denitrifiers) are affected by numerous
factors, especially the vegetation, the aeration and the mois-
ture status of the soil (Abou Seada and Ottow 1985;
Chapuis‐Lardy et al. 2007;Mojeremane2013; Serrano-
Silva et al. 2014). Finally, the bacteria and archaea that
thrive in the rhizosphere of wetland plants constitute an
important link in the food web, hosting viruses and feeding
bacteriovorous biota (Curl and Harper 1990).
The role of root exudates in the life of rhizosphere organ-
isms, the communication and interactions between organisms
and the roots and the techniques available for their study, have
all been described and reviewed mainly for dry soils (Bais et
al. 2004;Dennisetal.2010; Philippot et al. 2013). Such stud-
ies in wetland soils have targeted mainly the economically
important paddy rice (Colmer and Bloom 1998;Nishiuchiet
al. 2012). Wetland roots influence bacterial processes in the
outer region of their rhizospheres by modifying the availabil-
ity of substrates and providing oxygen and degradable organic
matter (Smith and Delaune 1984; Abou Seada and Ottow
1985; Bardgett and van der Putten 2014). The recently de-
scribed Bcable bacteria^can extend the rhizosphere (Nielsen
and Risgaard-Petersen 2015). Roots control the microbial en-
vironment of their rhizosphere, through a two-way exchange
with the soil of oxygen, CO
2
, nutrients and biochemicals
(Risgaard-Petersen and Jensen 1997; Kowalchuk et al. 1998;
Bodelier 2003). Oxygen released from the roots stimulates the
microbial oxidation of ferrous iron and ammonia; the products
of these processes can feed the plant and its rhizosphere biota
(Ehrenfeld et al. 2005;Herrmannetal.2008; Han et al. 2014).
Roots influence the emission of methane and other gases from
wetland ecosystems by altering their microbial production,
consumption and transport in the soil (Koelbener et al.
2010). On the other hand, microbial respiration competes with
other oxygenic processes and reduces the volume of the oxic
rhizosphere (Armstrong 1978; Armstrong et al. 1991;
Philippot et al. 2013). Microbially-released organic acids
and enzymes reactivate refractory nutrients and make them
available to the root (e.g., Craven and Hayasaka 1982;
Wetzel 1991). Anaerobic processes, like denitrification, N-
fixation and methanogenesis, usually take place further away
from the root (Faußer et al. 2012;Görresetal.2013).
The rhizosphere transmits information between organisms
by biochemical signals (such as nutrients, jasmonic acid,
salicylic acid and ethylene), which can modify biogeochemical
and biological processes (Lynn and Chang 1990;Baisetal.
2004; Herrmann et al. 2008; van Dam 2009;Faulwetteretal.
2009; Hinsinger et al. 2009; Laanbroek 2010; Nishiuchi et al.
2012; Han et al. 2014;Zengetal.2014). Bioactive chemicals
secreted by the roots of wetland plants (reviewed in Neori et al.
2000) probably predispose the microbial communities in favor
of the plant (reviewed in Curl and Truelove 1986; Gunnison
and Barko 1988a; Gunnison and Barko 1989;Westonetal.
2014). The understanding of the mutual inhibition performed
by rhizosphere organisms has found a practical use of the
effect in pest control (Sneh et al. 1977; Shieh and Simidu
1986; Smith et al. 1989). Microbial aerobic respiration near
the root and anaerobic respiration farther away modify root
exudates. The products diffuse back to the root and away from
it (Yoshida and Suzuki 1975; Federle and Schwab 1989).
Wetland plants encounter harmful soil toxins (Kinsman‐
Costello et al. 2015), among them Selenium, which can be
volatilized through methylation by rhizosphere microorgan-
isms (Azaizeh et al. 2003). Bacteria and archaea produce the
most important soil toxins, hydrogen sulfide, whose produc-
tion is coupled to microbial decomposition of organic matter
especially in the sulfate-rich salt marshes. Its inhibition by
oxidized conditions limits sulfate-reduction in the rhizosphere
(Wu et al. 2013). Sulfide inhibits the metabolism of plants
Wetlands (2017) 37:615–633 619
even at low concentrations (Pezeshki et al. 1988; Bradley and
Dunn 1989;Pulich1989;Kochetal.1990;Pezeshkietal.
1991;Mülleretal.1994). Adapted plants overcome this tox-
icity and thrive in salt marshes thanks to the opposing gradi-
ents of oxygen and sulfide in their rhizospheres (e.g.,
Andersen and Kristensen 1988). As sulfide diffuses toward
the root, it is microbially oxidized using oxygen and nitrate.
Sulfur bacteria, such as the chemolithotroph Beggiatoa spp.,
glide into optimal position within the opposing gradients of
sulfide and oxygen in salt marsh rhizospheres and intercept
the sulfide flow toward the root (Joshi and Hollis 1977;
Dickinson 1983; Good and Patrick 1987;Hedgesand
Messens 1990). The roots of certain wetland plants can also
oxidize sulfide in their tissues (Carlson and Forrest 1982;
Pearson and Havill 1988). Roots can regulate sulfate reduction
and sulfide oxidation in their rhizosphere through the control
of oxygen concentration, redox potential and exudate chemis-
try (McKee et al. 1988; Sidorenko 1989;Husson2013). The
release of low N exudates (such as sugars) and the uptake of
inorganic nitrogen suppresses sulfide generation near the root
(Sidorenko 1989).
The Metabolism of Nitrogen
Nitrogen occurs in the salts of ammonium (NH
4+
), nitrite
(NO
2
−
) and nitrate (NO
3
−
), and in the gases dinitrogen (N
2
),
nitrous oxide (N
2
O), nitric oxide (NO
2
and N
2
O
4
) and ammo-
nia (NH
3
). The conditions in the rhizosphere encourage the
enrichment of N-metabolizing microorganisms, owing to the
supply of organic matter and oxygen from the root, the steep
chemical gradients in the rhizosphere and the flow of various
nitrogenous molecules from the bulk soil into it (Faulwetter et
al. 2009;Lamersetal.2012; Trias et al. 2012;Yangetal.
2012). Bacteria and archaea in the wetland rhizosphere trans-
form nitrogen between its various forms by ammonification,
nitrification, assimilatory and dissimilatory denitrification (ni-
trate reduction), uptake, ANAMMOX (anaerobic ammonia
oxidation by nitrate) and N-fixation (concisely reviewed in
Vym a za l 2007; Bañeras et al. 2012). Some of these processes
require metabolic energy, obtained from organic matter oxida-
tion and lithotrophy; others release metabolic energy, which is
used by other processes.
Much of the wetland’sN-metabolismoccursatornearthe
rhizoplane (Good and Patrick 1987; Kirk and Kronzucker
2005; Hinsinger et al. 2009; Shen et al. 2012; Trias et al.
2012). The different N transformations are often coupled.
Roots supply oxygen to ammonifiers, which deaminate pro-
teins. The produced ammonia is taken up by the root or used
as an energy source by nitrifiers, which oxidize it to nitrite and
nitrate. The oxidized N diffuses to the root or away from the
oxic zone to denitrifiers, which in the absence of oxygen re-
duce nitrate to N
2
gas in the oxidation of organic matter and
mineralization of nutrients (Reddy et al. 1989). Reactive
nitrogen can be produced from non-reactive N
2
by microbial
N-fixation, a process that will be described here in more detail
because of its unique contribution to the global N-balance.
Microbial N-fixation is the chief natural source of reactive
nitrogen for the biosphere and for agriculture and is typical
to the natural and agricultural (rice and legumes) wetland eco-
system (Arima and Yoshida 1982;Gallowayetal.1995;
Vitousek et al. 2002).
Bacterial N-Fixation
N-fixation, which is performed by the nitrogenase enzyme in
heterotrophic and autotrophic prokaryotes, supplies the bio-
sphere with a large fraction of its reactive nitrogen require-
ments (Agami and Waisel 1986;Vitouseketal.2002). Light-
dependent N-fixation by cyanobacteria in wetlands is associ-
ated with the light-exposed regions (Vitousek et al. 2002)and
will not be discussed here. The taxonomy of the organisms
that perform heterotrophic N-fixation has been described in
detail (Young 1992; Lindström et al. 2015). Azospirillum,
Enterobacter, Klebsiella, Pseudomonas and Vibrio stand out
as important N-fixing bacterial genera (Shieh et al. 1987;
Shieh et al. 1988; Gunnison and Barko 1989; Shieh et al.
1989;Lamersetal.2012; Ormeño-Orrillo et al. 2013).
Heterotrophic N-fixers are usually engaged with roots in a
mutual symbiosis, exchanging root sugars for bacterially-
produced ammonia; many wetland plants (notably paddy rice)
depend on this ammonia because their soils are often N-
depleted by denitrification (Curl and Truelove 1986; Grant
et al. 1986;O’Donohue et al. 1991; Vitousek et al. 2002;
Ormeño-Orrillo et al. 2013). The plants accelerate N-fixation
several fold relative to non-vegetated areas (Arima and
Yoshi d a 1982; Curl and Truelove 1986; Howarth et al.
1988a,b; Hicks and Silvester 1990; Sengupta and
Chaudhuri 1991;Lamersetal.2012;Oyewole2012;
Bodelier and Dedysh 2013; Ormeño-Orrillo et al. 2013), es-
pecially in the less oxygenated regions of the wetland plant
rhizospheres (Arima and Yoshida 1982). However, the pro-
cess has also been discovered near and inside roots, with a
physical or temporal separation from oxygen (Whiting et al.
1986; Gunnison and Barko 1989; Vitousek et al. 2002). N-
fixation and denitrification, possibly affected by the same bac-
teria (Knapp 2012), often take place simultaneously in the
vicinity of the roots of rice and other plants (Arima and
Yosh i d a 1982). Paddy rice crop economics and sustainability
depend considerably on N-fixation, whereas other cereals re-
quire N fertilization (Grant et al. 1986;Kalininskaya1989;
Roger et al. 1991; Vitousek et al. 2002;Oyewole2012;Shu
et al. 2012).
The N-fixing process requires certain levels of pH and dis-
solved organic matter, Fe and Mo and is inhibited by oxygen,
nitrogenous nutrients, heavy metals and sulfate (Doremus
1982;Ogan1982; Howarth et al. 1988a,b; Kalininskaya
620 Wetlands (2017) 37:615–633
1989; Knapp 2012). The process has been documented in
rhizospheres of numerous non leguminous wetland plants,
while wetland legumes, like their terrestrial kin, contain sym-
biotic N-fixing bacteria (rhizobia) within their root nodules
(Dickinson 1983; Gunnison and Barko 1988a,b;Gunnison
and Barko 1989; Metting 1990;Zuberer1990;Oyewole
2012). Common non leguminous aquatic macrophytes that
harbor N-fixing bacteria on their roots or in their rhizosphere
include Halodule wrightii,Juncus balticus,J. effusus,
Phalaris arundinacea,Phragmites australis,Sagittaria
trifolia,Spartina alterniflora,Thalassia testudinum,Zostera
marina,Z. novazelandica as well as plants from the mangrove
genera Acanthus,Avicenni a,Bruguiera,Ceriops,Rhizophora
and Sonneratia (Patriquin and Keddy 1978;Ogan1982;
McClung et al. 1983; Gunnison and Barko 1989; Shieh et
al. 1989;HicksandSilvester1990; Waisel and Agami 1991;
Knapp 2012).
Roots promote N-fixation by depleting nitrogen from their
rhizosphere, exuding low-N organic matter and optimizing the
levels of pH and redox potential (Husson 2013). Rice’sorgan-
ic exudates also specifically stimulate the nitrogenase activity
in heterotrophic N-fixers, but not in cyanobacterial N-fixers
(Habte and Alexander 1980; Vitousek et al. 2002). N-fixing
microorganisms, such as Azospirillum, move along the rhizo-
sphere’s chemical gradients (especially oxygen and NH
4
), re-
lease root- stimulating hormones (auxins), and manipulate
rhizosphere pH and redox potential to optimize their activity
(Hemming 1986; Oyewole 2012).
Fungi - General
Fungi associate intimately with roots in wetland plant rhizo-
spheres and thereby impact prominently wetland functioning
(Peat and Fitter 1993; Anderson and Cairney 2007;Kohoutet
al. 2012;Krishnakumaretal.2013; Twanabasu 2013; Shah
2014). Multi-level physical, chemical, hormonal and genetic
interactions between roots, fungi and other rhizosphere organ-
isms are prevalent and often species-specific (Koske 1982;
Pennington 1986; Gunnison and Barko 1988a; Hutchison
and Piché 1995;Wangetal.2011; Burke et al. 2012;
Kohout et al. 2012). Concentration gradients in oxygen and
organic exudates attract fungi toward the rhizosphere, where
they can feed and grow (Lee and Baker 1973; Armstrong
1978;Dickinson1983; Hutchison and Piché 1995; Wang et
al. 2015). The wetland rhizosphere’s fungal community,
which is denser, more diverse and genetically different com-
pared to bulk unvegetated wetland soil communities, can be
influenced by plant species, soil, climate, water saturation re-
gime and other soil organisms (Dolinar et al. 2010;Mohamed
and Martiny 2011). Fungal-plant associations perform several
specialized functions (Ehrenfeld et al. 2005; Wenzel 2009;Liu
et al. 2015), such as Fe nutrition and metal detoxification by
the emission of metal-chelating siderophores (Hemming
1986;Sahaetal.2015) and denitrification (Liu et al. 2015).
Mycorrhizal Fungi
Mycorrhizal fungi, which belong to the phylum
Glomeromycota (Redecker and Rabb 2006), form mutualistic
symbiotic associations with roots; ectomycorrhizal fungi
(some of whose above-ground fruiting bodies we call mush-
rooms) form a mat outside the root, and penetrate only the
intercellular spaces; arbuscular mycorrhizal fungi (currently
abbreviated as AMF or AM, and VAM - vesicular-arbuscular
mycorrhiza - in older literature) are endomycorrhizal, i.e. they
live inside the living cells of the root cortex (Brundrett 2006).
Analogous to rhizodeposition by the roots, the fungal hyphae
surround themselves with a mycorrhizosphere through the
hyphodeposition process (Ellouze et al. 2011).
The mycorrhizal symbiosis supplies the dry-soil plant with
resources (especially water and nutrients), expands the colo-
nized soil volume, fights pests, synergizes with beneficial or-
ganisms and dissipates pollutants (Brundrett 2006). It also
enhances soil quality and stability, carbon transport and the
activity of soil invertebrates; the fungus is rewarded with root
exudates and oxygen (Brundrett 2006; Krishnakumar et al.
2013). The AM infection rate is higher in low-phosphorus
sediment, where the fungi seem to extract phosphorus from
solid phase fractions that are normally not available to plants
(Smolders et al. 2002). While AM infection may help wetland
plants in obtaining soil phosphorus under P-limitation
(Cornwell et al. 2001; Smolders et al. 2002), usually, the fun-
gal assistance in supplying the plants with nutrients and water
is probably unnecessary in wetlands. Nevertheless, the re-
maining benefits of the symbiosis are valuable enough on their
own, judging from the high correlation between the level of
AM infection and the rate of land colonization and growth by
various wetland plants (Anderson et al. 1984; van Duin et al.
1989; Wirsel 2004; Gutknecht et al. 2006; Stevens et al. 2011;
Twanabasu 2013;Wangetal.2015). A contribution of AM-
infection to the success in transplanting wetland plants was
observed long ago and was linked to improved nutrient trans-
port through the roots’cytoplasmic membranes, whose per-
meability decreases in flooded soils (Mason 1928). AM im-
prove the water-and-salt equilibrium in salt marsh plants
(Rozema et al. 1986) and also enhance plant growth in
peatlands (Andersen et al. 2013). AM influence plant commu-
nity structure by altering the host plant’s physiology, mediat-
ing competitive interactions between plants and influencing
the soil microbial community structure (Twanabasu 2013).
In orchids, both in wetlands and elsewhere, the fungi provide
both inorganic and organic nutrition, at least during the non-
pigmented life stage (Brundrett 2006).
Mycorrhizal colonization, mostly of the arbuscular type, is
prevalent in most wetland ecosystems, including cypress
Wetlands (2017) 37:615–633 621
swamps, bottomland hardwood forests, nutrient-poor fens,
tropical river flood-plains and tropical marshes (reviewed in
Twanabasu 2013). AM-infection prefers less anoxic soils, in
paddy rice (Kohout et al. 2012;Oyewole2012;
Watanarojanaporn et al. 2013) and in many other wetland
species (Bagyaraj et al. 1979; Chaubal et al. 1982;
Anderson et al. 1984;Bagyaraj1984; Clayton and Bagyaraj
1984; Pennington 1986; Lodge 1989;Rogeretal.1991;
Rickerl et al. 1994; Peterson et al. 2004; Gutknecht et al.
2006; Robertson et al. 2006; Anderson and Cairney 2007;
Dolinar et al. 2010; Mohamed and Martiny 2011;
Twanabasu 2013; Twanabasu et al. 2013;Shah2014;
Moche et al. 2015). Interestingly, however, AM infection in
aquatic plants is rare in roots rich with root hair (Søndergaard
and Laegaard 1977; Clayton and Bagyaraj 1984; Peat and
Fitter 1993), like the Juncaceae and the Cyperaceae
(Dickinson 1983). On the contrary, the root hair-less isoetid
macrophytes, which grow in nutrient-poor wetlands, are AM-
infected (Farmer 1985; Agami and Waisel 1986;Smolderset
al. 2002;Brundrett2006).
The transmission of the obligate symbiotic mycorrhizal
fungi to new hosts occurs through the extension of hyphae
toward the uninfected root and by the transfer of resting spores
through the soil; the sensitivity of the fungal hyphae and
spores to low redox potential limits the infection mode in
highly-reduced wetland soils to a physical contact between
the rhizospheres of the infecting and the infected plants; this
hampers the colonization of new wetland habitats by AM-
dependent plants (van Duin et al. 1989; Gutknecht et al.
2006).
Protozoa
Protozoa are widespread in wetland rhizospheres, where their
feeding on roots and microorganisms enhances, on the one
hand, nutrient cycling through the microbial loop and, on the
other hand, facilitates the passage of nutrients and energy up
the food chain to larger organisms and to higher trophic levels;
furthermore, their movement physically transports nutrients
and bacteria within the rhizosphere (Hemming 1986;
Bamforth 1988; Dart 1990;Niederlehner and Cairns 1990a,
b; Raven et al. 1990;Vargas1990; Uikman et al. 1991;
Schönborn 1992; Verhagen et al. 1993; Bonkowski et al.
2009;Crottyetal.2012). Unfortunately, even though the
number of publications that mention ‘protozoa’has grown
dramatically in recent decades (Table 1), we still lack quanti-
tative data on the functioning of protozoa in this environment
(Bamforth 1988;Crottyetal.2012). While the majority of the
surveyed ‘protozoa’publications in Table 1concerned paddy
rice, only a handful of them focused on the rhizosphere (Roos
and Trueba 1977;Madoni1987; Jousset et al. 2008;Murase
and Frenzel 2008;Oyewole2012).
Larger Organisms –General
Soil animals include nematodes, enchytraeids,
microarthropods and larger fauna (termites, millipedes,
earthworms and even larger animals; Stirling 2014). The spe-
cific role that these animals play in wetland functioning can be
understood chiefly from studies in rice (Kimura 2005;Stirling
2014). Evidently, the wetland rhizosphere attracts small ani-
mals with its oxygenic environment, food of diverse trophic
levels and sizes, habitat complexity, physical protection and
synergism with other organisms (Mason and Standen 1983;
Speight and Blackith 1983; Curl and Harper 1990;Hinsinger
et al. 2009; Leduc and Probert 2011;Ohtakaetal.2011;
Ohtaka et al. 2014). Only invertebrates will be discussed here.
Invertebrates
Invertebrates in wetland soils are attracted to the rhizosphere
by the same factors that attract microorganisms, like oxygen
and food (Jousset et al. 2008;Bonkowskietal.2009).
Rhizosphere invertebrates function ecologically like the pro-
tozoa, in consuming exudates, biota, flora and root tissue,
modifying microbial biogeochemical processes, moving and
recycling nutrients, and influencing plant growth (Bird and
Jenkins 1965;Inghametal.1985; Griffiths 1989,1990;
Cohn and Spiegel 1991; Mao et al. 2011; Du et al. 2014).
They can also be afflicted by fungi, parasites and predators
(e.g., Stirling 2014). The roots and the dense populations of
rhizosphere microorganisms feed many invertebrates
(Hinsinger et al. 2009; Leduc and Probert 2011) and thereby
lead to a correlation between the distribution of plant roots in
different wetland environments and the distribution of soil
invertebrate, including herbivores and predators (Moran et
al. 1988;Gerson1991;LanaandGuiss1991; Sagova et al.
1993;Liaoetal.2015). It could be a typical bottom-up control
(Moore et al. 2003), but the grazing of invertebrates on smaller
organisms diminishes the wetland’s microbial community
(Mason and Standen 1983; Speight and Blackith 1983;
Carpenter and Lodge 1986; Roger et al. 1991;Sillimanand
Bertness 2002; Bonkowski et al. 2009), i.e., a top-down con-
trol (Moore et al. 2003). Apparently, there is no general an-
swer with respect to the wetland rhizosphere, since even
though both types of trophic control have been established
in different wetlands, none of these studies targeted rhizo-
sphere invertebrates (Batzer 2013).
Animal life in the anaerobic soil involves special adapta-
tions, such as a high content of hemoglobin as well as air sacs.
These adaptations bring invertebrate density in wetlands to
thousands and millions of individuals m
−2
(Grant et al.
1986). Peat invertebrates congregate near roots (Speight and
Blackith 1983), where they are more numerous but of a small-
er individual size and species diversity compared to other soils
(Mason and Standen 1983). Overall, detritivorous animals
622 Wetlands (2017) 37:615–633
(oligochaetes and dipterids), mites, Collembola and nema-
todes are the abundant invertebrates in peat (Mason and
Standen 1983; Dvorak 1987; de Szalay and Resh 2000).
Copepods, cladocerans, coleopterans, rotifers, ostracods, chi-
ronomid larvae and molluscs are also found in wetlands, such
as rice paddies; tubificid worms and chironomid larvae influ-
ence the functioning of wetlands by their burrowing, which
enhances nutrient and gas exchange in the otherwise stagnant
flooded soils (Kinsman‐Costello et al. 2015). Animals also
release extracellular enzymes that digest organic matter
(Prejs 1977; Prejs 1986b; Wetzel 1991). Animals accelerate
nutrient movement, mineralization and recycling, and thereby
modify the rhizosphere’s chemistry and biology (Mason and
Standen 1983; Curl and Harper 1990; Ettema et al. 1998;
Neher et al. 2005; Ohtaka et al. 2011; Bardgett and van der
Putten 2014;Ohtakaetal.2014). For instance, the grazing of
N-fixers by invertebrates can reduce the N supply, diminish
the crop and favor grazer-resistant mucilaginous
cyanobacteria in rice paddies (Grant et al. 1986).
The quantitative information related to the interactions be-
tween wetland characteristics (type, soil and plant) and the
specific rhizosphere’s invertebrates is limited (Carpenter and
Lodge 1986; Stirling 2014), becasue most studies have fo-
cused on communities rather than on the functioning of indi-
vidual species in food chains (Paoletti et al. 1991; Ohtaka et al.
2011; Ohtaka et al. 2014).
Nematodes constitute one of the most abundant and diverse
groups of soil (dry and wet) fauna (Mason and Standen 1983;
Dvorak 1987; de Szalay and Resh 2000; Neher et al. 2005;
Hodda et al. 2009; Nielsen et al. 2014). Prejs (1977,1986a,b,
1987), Mason and Standen (1983), Agami and Waisel (1986)
and Waisel and Agami (1991) described a handful of studies
on wetland nematodes. For instance, 3 × 10
6
animals (up to
750 mg of biomass) were extracted from 1 m
2
of Juncus
aquarrosus stand (Mason and Standen1983). Nematodes live
and move in water (Neher 2010), a feature which probably
contributes to the dependence of total nematode abundance on
soil moisture (Nielsen et al. 2014). Most soil nematodes feed
on bacteria, fungi and detritus, while othersbut some also feed
on algae, while others are algivores, obligate rhizovores, pred-
ators or omnivores (Mason and Standen 1983; Neher et al
2005; Nielsen et al. 2014). Their size and abundance make
nematode populations excellent biological indicators of soil
that depend on quantifiable linkages between indicator taxa
and ecosystem function (Neher 2010; Okada et al. 2011).
Nematodes in rice rhizosphere have naturally received more
attention than in other wetlands (Ebsary and Pharoah 1982;
Cuc and Prot 1992;Protetal.1994).
Free-living nematodes prefer sediments overgrown with
macrophytes (Prejs 1977). Root oxygen allows rhizovorous
nematodes to live deeper underground than nematodes of the
bulk wetland soil (Nicholas et al. 1991; Okada et al. 2011;Yan
et al. 2012). Many species of phytoparasitic and free-living
nematodes are associated with the roots of common wetland
plants (e.g., Esser et al. 1985). However, the ecological func-
tioning of such wetland nematodes has been insufficiently
studied (Neher et al. 2005; Neher 2010; Bardgett and van
der Putten 2014), even though the knowledge of their
macroecology and biogeography has greatly advanced in re-
cent years, particularly through the development of sophisti-
cated molecular techniques (Nielsen et al. 2014).
Complex Interactions and Symbioses
Complex and manifold interactions have been described be-
tween the roots of wetland plants and their surrounding soil
and biota (e.g., Chaudhuri et al. 2014). The functioning of the
vegetated wetland is considerably influenced and even char-
acterized by the dominant plants and their interactions with
the soil, nutrients and the soil-borne organisms, especially
mycorrhizal fungi, root-feeding invertebrates and root patho-
gens; root exudates stimulate important groups of microbes in
the rhizosphere that are involved in the various nutrient cycles,
attract beneficial organisms by chemical signals and inhibit
pests (Schippers et al. 1986; Brix 1987; Neori et al. 2000;
Hairiah et al. 2001; Ehrenfeld et al. 2005; Ravit et al. 2006;
Vohník et al. 2009; Kuzyakov 2010; Stout and Nüsslein 2010;
Coleman 2011; Husson 2013; Bardgett and van der Putten
2014). Chemical, hormonal and genetic multiple-way interac-
tions and stimulations between the roots, their rhizosphere
biota and their chemistry are rarely studied in wetlands, how-
ever (Neori et al. 2000; van Dam 2009;Lamersetal.2012).
Existing information about these interactions is inadequate for
any soil type, but this inadequacy is particularly noticeable in
flooded soils (Rusek 1992; Doyle and Otte 1997; Devereux
2005; Bezbaruah and Zhang 2006;Feeneyetal.2006;
Blossfeld et al. 2011; Vymazal 2011; Balasooriya et al. 2013).
Many soil invertebrates, in both drylands and wetlands,
simply feed in the rhizosphere (Heckman 1994;Bonkowski
et al. 2009). However, root-microbe-fauna relationships and
feedback in wetlands often have additional features of higher
hierarchies, primarily related to issues such as the aforemen-
tioned oxygen and water saturation, toxins, bioactive
chemicals and the biochemical uniqueness of the wetland rhi-
zosphere (Brix and Schierup 1990; Armstrong et al. 1992;
Neori et al. 2000). The wetland organisms often depend on
roots or on their exudates, but while water-carried substances
and organisms are moved and exchanged more freely between
the roots and the bulk soil in flooded soils compared to dry
soils, diffusion of gases like oxygen and CO
2
is slower in
flooded soils (Hinsinger et al. 2009; Jarvis et al. 2013;Han
et al. 2014;Larsboetal.2014).
Symbiotic interactions between aquatic species sometimes
involve the ‘culture’of one by another (Margulis 1981). Well-
known symbiotic examples are Rhizobium development with-
in legumes, prochlorophytes growth within invertebrates,
Wetlands (2017) 37:615–633 623
zooxanthellae within hard corals or molluscs, luminescent
bacteria in animals (Smith 2001) and cyanobacteria in marine
microalgae and protozoa (Kimor et al. 1992). However, ex-
amples that are specific to wetland rhizospheres, in addition to
the aforementioned mycorrhizal fungi, involve mainly chem-
ical and genetic interactions between roots and pathogens in
agriculture crops (Dixon and Lamb 1990;reviewedinNeoriet
al. 2000;Hartmannetal.2009; Sanon et al. 2009; Sessitsch et
al. 2012; Nelson and Karp 2013).
Early research that integrated rhizosphere microbiological
processes, animals and interactions has been reviewed in sev-
eral articles (Carpenter and Lodge 1986; Gunnison and Barko
1988a,b; Gunnison and Barko 1989; Barko et al. 1991;
Wais el and Aga m i 1991;Maberly2014). The current litera-
ture about complex interactions in man-made wetlands, either
paddy rice or constructed wetlands (Coats and Rumpho
2014), allows an extrapolation to the natural wetlands.
Multiple mutualistic and antagonistic interactions are preva-
lent between microbes, animals and plants in terrestrial rhizo-
spheres (Elad 1986; Hinsinger et al. 2009). Such interactions
include the release of bioactive metabolites, siderophore che-
lation, microbial parasitism on pathogens and food competi-
tion (Hemming 1986; Schippers et al. 1986; Bakker and
Schippers 1987; Lynch 1990;Oyewole2012).
Conclusions and Recommendations for Further
Research
Rhizosphere soils are hot spots of biotic activity of unique
organisms, from viruses to arthropods. The biota of the soil
in the wetland rhizosphere often dominates the functioning of
the entire ecosystem, with respect to individual number, di-
versity, biomass and biochemical activity. Complex interac-
tions between soil, roots, interstitial water, chemicals and or-
ganisms, create steep gradients. Thanks to their larger size,
animals could hypothetically transverse through and make
use of these gradients to enjoy the two worlds, i.e., the oxi-
dized root and the anaerobic soil.
The wetland rhizospheres contain specialized microbial
and animal populations, which live in symbioses and have
various interactions with each other and with the roots. Our
understanding of the wetland is incomplete as long as we do
not understand these interactions. Publications in the last two
decades have reported a growing yet still insufficient number
of multidisciplinary studies probing and understanding how
the complex communities of rhizosphere biota are distributed
in the wetland soil, and how they function and impact the
vegetation and the biogeochemical cycles in the wetland.
A rising interest in wetlands, together with the overcoming
of the technical challenges posed to scientists by multidisci-
plinary studies in the wetland rhizosphere, probably account
for this development. However, surprisingly few studies have
examined the signaling and communication between the liv-
ing members of the rhizosphere biota, in-spite of their presum-
ably large impact on the functioning of the wetlands and on
the global environment (Bais et al. 2004; Gutknecht et al.
2006; Bonkowski et al. 2009; Pii et al. 2015). For instance,
the complex control exerted by plants, microorganisms and
invertebrates on wetland methane and nitrogen metabolism
may influence global greenhouse gas emissions (Dingemans
et al. 2011;Wangetal.2012).
ABbig picture^of the soil, water, plants, chemicals and
biota in the rhizosphere, as well as of the processes in which
they participate and the temporal and spatial dynamics of the
rhizosphere interactions, seems to still be out of reach. We
anticipate that this void will be filled by applying to natural
wetlands the scientific approaches that were used so success-
fully in studies of rhizospheres in man-made wetlands and in
dry soils (e.g., Bazin et al. 1990; Chaudhuri et al. 2014). The
methods developed for the study of aquatic viruses
(Weinbauer and Rassoulzadegan 2004; Jacquet et al. 2010)
could also be of assistance in the study of rhizosphere viruses
and their quantitative functions in wetland rhizospheres.
The present review highlights research challenges for the
future, and also proposes a course for advancing an understand-
ing of the role of rhizosphere biota in determining the function-
ing of the wetland and its role in global processes. Several
features could aid multi-disciplinary studies in wetlands: (1)
diverse groups of organisms and processes within the rhizo-
sphere function in defined zones; (2) water and gases that me-
diate the main chemical interactions are easy to sample; (3) the
organisms are less mobile in their position relative to one other
compared with aquatic habitats; (4) core samples of the entire
wetland ecosystem (plants, soils and biota) can be extracted and
moved to the laboratory, with little loss of functioning; (5)
conceivably, several types of wetlands, with their unique soil,
water regime, plant species, climate etc. can be recreated arti-
ficially in controlled environments, such as phytotrons.
Chemical- and genetic- oriented studies that utilize these ad-
vantages can open the Bblack box^of the wetland rhizosphere
(Gutknecht et al. 2006; Andrén et al. 2008; Coleman 2011;
Gärdenäs et al. 2006). The physico-chemical and genetic char-
acteristics of the different zones that exist around the plant’s
root can be characterized and then used to understand the in-
teractions between the rhizosphere’s chemistry, physics and
biota. Extracts from the different zones (including the root it-
self) as well as selected fractions of these extracts can help to
characterize molecules with specific biological impacts on bi-
ota and plants. The ecological relevance of interesting mole-
cules with respect to the functioning of the wetland can then be
further studied in different ways. Microelectrode studies can
measure in micro- and nano- detail the various gradients and
their associated biogeochemical processes, perpendicular to the
roots (see in Andersen and Kristensen 1988; Højberg and
Sørensen 1993;Wangetal.2015).
624 Wetlands (2017) 37:615–633
Modern chemical and genetic sampling and analyses and
culture-independent molecular technologies for community
analysis (Buyer 1995;Jacobsen1995;Uedaetal.1995;
Laanbroek 2010; Blazejak and Schippers 2011;Wangetal.
2011;Churchlandetal.2012; Mei et al. 2012;Pesteretal.
2012; Shade et al. 2012; Shu et al. 2012;Duanetal.2013;
Chaudhuri et al. 2014) can greatly increase our comprehen-
sion of the microbial variety that exists across the rhizosphere
(Anderson and Cairney 2007).
Wetlands provide us with a wide array of interesting, excit-
ing, complex and globally important scientific challenges.
Meeting these challenges requires well-funded and well-
staffed multi-disciplinary research programs that combine
the most advanced technologies in order to integrate into the
understanding of wetland ecosystems the impacts that the rhi-
zosphere biota has on the wetland–one of the most active,
most complex and, globally, most important ecosystems in
existence.
Acknowledgments Much of this review was prepared during visits of
AN at the University of Florida, Tel Aviv University, Bar Ilan University,
University of California San Diego (library of Scripps Institution of
Oceanography) and the Institutes of Botany and of Microbiology -
Academy of Sciences of the Czech Republic, Třeboň. The early and grey
literature was assembled chiefly with the help of K Brown and the
University of Florida’s UF/IFAS Center for Aquatic and Invasive Plants
and the staff of the UF Marston Science Library, in Tel Aviv University’s
Botanical Garden and in the library of the Institute of Botany, Třeboň.We
thank H Čížková-Končalová, J Květ, ŠHusák, O Lhotský, BG Mithell
and KR Reddy for their encouragement and for the useful discussions
they provided. We further thank Wetlands Editor, an anonymous reviewer
and L Baumer for their seminal contributions in substance and form to the
manuscript.
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