Abstract
Microbiota play essential roles in
nitrogen (N) cycling in freshwater river ecosystems. However, microbial
functional groups associated with N cycling (especially denitrification)
in freshwater rivers under anthropogenic disturbance are still poorly
understood. Here, we studied the
impacts of different land-use types on denitrification-related microbial
communities in Weihe River, Hanjiang River, and their tributaries, in
the Qinling Mountains, China. The major land-use types in the three
river areas were divided into natural (forest, shrub, grassland, and
open water) and anthropogenic (agricultural and urbanized land) types. A
landscape survey of microbiota in the river water and sediment was
carried out with extensive sample sources
based on deep 16S rRNA gene
sequencing, which yielded operational taxonomic units for predicting
functional groups. With increases
in proportions of agricultural and urbanized land areas, electrical
conductivity, total N, ammonium-N, and
nitrate-N all increased in water
samples. Conversely, microbial diversity exhibited a decreasing trend in
water samples, whereas the relative abundance of denitrification-related
functional groups increased, with increases in the proportions of
agricultural and urbanized land areas. The relative abundances of
denitrification- and human-related microbial functional groups in
sediment samples were distinctively higher in Weihe River (mainly under
agriculture and urbanization), when compared with those of Hanjiang
River and Qinling tributaries (dominated by forests).
The results indicate that
anthropogenic land-use types, such
as agricultural and urbanized land, result in simple microbial community
structure and stimulate microbe-mediated denitrification in freshwater
rivers.
Keywords: Land-use type,
Denitrification, Microbiota,
Freshwater ecosystems,
Agricultural
land, Urbanized land
Background
Freshwater is a fundamental component of aquatic ecosystems and is
essential for coupling of biogeochemical cycles between continents and
oceans (Aufdenkampe et al., 2011). The
emission of
greenhouse gases (GHG) from
freshwater
ecosystems is source of concern globally (Searchinger et al., 2008,
Robertson et al., 2000 and Liu et al., 2020). Freshwater systems emit
0.3 Tg N yr−1 to the atmosphere in the form of nitrous
oxide (N2O) under natural conditions (Tian et al.,
2020), with implications for global warming. N2O is one
of the most long-lived GHGs (Prinn et al., 2018). The atmospheric
N2O burden increased from 1,462 Tg N in the 1980s to
1,555 Tg N in 2007–2016, with anthropogenic N2O
emissions at 7.3 (4.2–11.4) Tg N yr−1 and natural
N2O emissions at 9.7 (8.0–12.0) Tg N
yr−1, respectively (Tian et al., 2020). Consequently,
it is essential to explore the mechanisms of nitrogen (N) cycling in
freshwater systems, which could facilitate the minimization of the
impacts of N2O emissions on global warming.
Microbiota play active roles in the conversion of N in freshwater
ecosystems (Mosier et al., 1998). Generally, organic N is transformed
into molecular N via two pathways. First, ammonium-N
(NH4+-N) is oxidized into nitrate-N
(NO3--N) or nitrite-N
(NO2--N) by nitrifying bacteria;
second, NO3--N or
NO2--N is reduced to gaseous N by
denitrifying bacteria (Shen et al.,
2021). In addition,
N
fixation refers to the reduction of N2 molecules to
NH3 or organic N by N-fixing bacteria (Ryu et al.,
2020). In freshwater environments, nitrification, denitrification, and N
fixation processes mediated by distinct microbiota establish the N cycle
alternately or simultaneously. The denitrification process produces
N2O as an intermediate. N2O emissions
are higher in areas with intense anthropogenic disturbance than in areas
with minor disturbance (Zhao et al.,
2021).
Microbiota as the foremost
decomposers in nature drive the decomposition of biological remains and
maintain biogeochemical cycling (Zaan et al., 2010 and Xu et al., 2014).
Microbiota colonize suitable environments (Harrison et al., 2014) and
respond sensitively to environmental stimuli, such as toxic substances,
sewage treatment, and natural self-purification (Pei et al., 2018 and
Wang et al., 2021). In addition, aquatic bacterial diversity is
influenced by evapotranspiration, elevation, and temperature (Zhang et
al., 2021). A large number of
denitrifying bacteria exist in
high-N
wastewater (Pai et al., 1999; Liu et al., 2020). In the past,
denitrification
was mainly considered to occur in anaerobic or hypoxic conditions;
however, recent studies have reported that some bacteria can also
perform
denitrification
under aerobic conditions (Wan et al., 2009). According to Alessandra
(2017), N2O emissions are released from the
hyporheic–benthic zone and benthic–water column zone in the Kalamazoo
River, Michigan, USA.
Anthropogenic disturbance disrupts the intensity, frequency, and timing
of natural disturbance regimes that maintain the ecological integrity of
river
ecosystems (Cabezas et al., 2009). River ecosystem characteristics are
often governed by interactions between hydrological connectivity and
local environmental conditions. Such interactions, coupled with
intensive
agricultural
and urbanized land uses, severely alter
river
hydrodynamic and biogeochemical gradients (Valipour et al., 2012 and
Campo et al., 2014). Despite the impacts of anthropogenic disturbance on
microbiota have been explored in marine and terrestrial ecosystems
(Archer et al., 2020), it remains unclear how different land-use types
influence microbial community structure in freshwater ecosystems.
Numerous factors influence microbe-mediated N cycling and
denitrification in aquatic ecosystems. For example, saltwater intrusion
can alter the interactions between biotic and abiotic components in
tidal wetland ecosystems and therefore influence denitrification rates
(Neubauer et al., 2019). Long-term sulfide inputs in freshwater lake
sediments enhance chemoautotrophic denitrification, rather than
dissimilatory NO3--N reduction into
NH4+-N (Ypa et al., 2021). However,
there is still a dearth of studies assessing the impacts of different
land-use types on denitrification efficiency and associated microbial
communities in freshwater river ecosystems.
The present study
evaluated
the impacts of different land-use types on the characteristics of river
environment, microbial community structure, and denitrification-related
functions in a freshwater ecosystem. The results of the present study
could offer novel insights into microbe-mediated denitrification in
freshwater rivers under anthropogenic disturbance.