GEOPHYSICAL RESEARCH LETTERS, VOL. 38, L21603, doi:10.1029/2011GL049095, 2011
Impact of ocean acidification on benthic and water column
ammonia oxidation
Vassilis Kitidis,1 Bonnie Laverock,1 Louise C. McNeill,1 Amanda Beesley,1
Denise Cummings,1 Karen Tait,1 Mark A. Osborn,2 and Stephen Widdicombe1
Received 1 August 2011; revised 23 September 2011; accepted 30 September 2011; published 2 November 2011.
[1] Ammonia oxidation is a key microbial process within the
marine N‐cycle. Sediment and water column samples from two
contrasting sites in the English Channel (mud and sand) were
incubated (up to 14 weeks) in CO 2 ‐acidified seawater
ranging from pH 8.0 to pH 6.1. Additional observations
were made off the island of Ischia (Mediterranean Sea), a
natural analogue site, where long‐term thermogenic CO2
ebullition occurs (from pH 8.2 to pH 7.6). Water column
ammonia oxidation rates in English Channel samples
decreased under low pH with near‐complete inhibition at
pH 6.5. Water column Ischia samples showed a similar
though not statistically significant trend. However, sediment
ammonia oxidation rates at all three locations were not
affected by reduced pH. These observations may be explained
by buffering within sediments or low‐pH adaptation of the
microbial ammonia oxidizing communities. Our observations
have implications for modeling the future impact of ocean
acidification on marine ecosystems. Citation: Kitidis, V.,
B. Laverock, L. C. McNeill, A. Beesley, D. Cummings, K. Tait,
M. A. Osborn, and S. Widdicombe (2011), Impact of ocean acidification on benthic and water column ammonia oxidation, Geophys.
Res. Lett., 38, L21603, doi:10.1029/2011GL049095.
1. Introduction
[2] Sustained observations and modeling studies have
shown that oceanic pH is currently decreasing by 0.02 units
per decade and is expected to decrease by up to 0.7 units by
the year 2100 as a result of atmospheric CO2 dissolution in
the oceans [Bates, 2007; Caldeira and Wickett, 2003; Olafsson
et al., 2009; Santana‐Casiano et al., 2007]. This ocean acidification (OA) is predicted to affect marine ecosystems through
the alteration of community structure [Fabry et al., 2008];
nutrient cycles [Hutchins et al., 2009]; productivity [Riebesell
et al., 2007] and carbon export [Mari, 2008; Schulz et al.,
2008]. Of significant concern is the potential impact of OA
on the processes involved in the biogeochemical cycling of
nitrogen (N) and, in particular, nitrification; a key microbial
process through which remineralized N in the form of
ammonia (NH3) is oxidized to inorganic nitrite (NO−2 ) and
subsequently to nitrate (NO−3 ). A number of recent and past
studies have demonstrated an inhibitory effect of decreasing
pH on water column nitrification activity [Beman et al., 2011;
Huesemann et al., 2002; Jones, 1992; Stein et al., 1997]. The
implications of such an effect on ecosystem function could be
1
2
Plymouth Marine Laboratory, Plymouth, UK.
Department of Biological Sciences, University of Hull, Hull, UK.
Copyright 2011 by the American Geophysical Union.
0094‐8276/11/2011GL049095
significant with modeling studies suggesting that substantial
reductions in water column nitrification over the next century
would affect nutrient stoichiometry, denitrification and by
extension marine productivity and the biological carbon pump
[Beman et al., 2011; Blackford and Gilbert, 2007]. However,
the impact of OA on nitrification within sediments has not been
examined. It is conceivable that alkalinity generation in sediments [Thomas et al., 2009] and/or low‐pH‐adaptation by
microorganisms may moderate the effects of decreasing pH on
nitrification in sediments. Here we test the hypothesis that
CO2‐induced acidification causes a reduction in water‐column
and surface‐sediment NH3 oxidation using data generated
from two controlled manipulative incubations and a set of
field‐measurements in the vicinity of natural CO2 vents.
2. Sampling and Methods
2.1. Experimental Manipulations
[3] Sediment was collected from Plymouth Sound (hereafter
PS; 50.35°N, 4.13°W) and the Eddystone shell gravel site
(hereafter ED; 50.19°N, 4.28°W) in the western English
Channel during January 2010 and September 2010 respectively. The ED station is characteristic of open continental shelf
regions while the PS site is characteristic of coastal waters that
are influenced by freshwater inputs. Sediments at these sites are
dominated by sand‐shell fragments (ED) and fine mud (PS). ED
and PS sediment cores (0.38 m height, 0.18 m diameter and
0.65 m height, 0.30 m diameter respectively) were kept under
seawater at ambient temperature (11.5 ± 1.3°C) and light
in the Plymouth Marine Laboratory mesocosm facility for 4–
6 days (ED) and 8 weeks (PS) prior to the start of experiments.
PS sediments stored for 8 weeks had similar NH3 oxidation
rates to ongoing measurements at this site (no storage). All
pH measurements were carried out in the overlying water
with a glass electrode pH‐meter (Metrohm, pH‐826) against
the NBS scale. For ED sediment incubations, overlying water
in the cores was flushed with seawater from five header tanks
(19 ± 9 mL min−1), with each tank acidified by purging with
CO2(g) to set pH values of 6.1, 6.7, 7.1 and 7.5. A control sample
of pH 8.0 was purged with air. Seawater for the header tanks was
topped up continuously from a master tank filled weekly with
seawater from the English Channel (salinity 33.8 ± 0.5). Header
tank pH, monitored weekly, fluctuated by <0.2 units in each
treatment over the course of the incubations. After two and ten
weeks replicate cores (3 and 4 cores respectively per pH
treatment) were removed for sampling. For the PS sediments,
replicate cores (n = 4 per pH treatment) were incubated for
14 weeks in 1 m3 tanks which were filled with seawater and
individually acidified with CO2(g) to pH values of 6.8, 7.3,
7.7, 7.9 and 8.1 (control). At the end of these incubations,
24‐hour slurry‐type incubations were set up in 14 mL glass
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Figure 1. Water column and benthic NH3‐oxidation under different pH treatments in samples from Plymouth Sound (PS),
the English Channel (ED; after 2‐ and 10‐weeks incubations) and from long‐term‐CO2‐exposed samples from Ischia Island
(Mediterranean Sea). Filled circles and grey squares represent NH3‐oxidation rates for individual cores and average rate per
treatment respectively (error bars indicate standard deviation of replicate cores; n = 3–4; error bars for individual cores are
too small to be seen at this scale).
vials with approximately 2/3 surface sediment (top 1 cm) and
1/3 seawater from the corresponding header tank in each vial.
A further set of vials was filled with header tank seawater
only, to determine NH3 oxidation rates in the overlying water.
Average NH3 concentration (0.15 ± 0.16 mmol L−1) did not
differ between pH treatments for our experiments. Aliquots
(0.1 mL) of 0.1 M allylthiourea (ATU) and sodium chlorate
(NaClO3) were added to separate vials (n = 3 per ATU/
NaClO3‐treatment, per core). ATU and NaClO3 are inhibitors
of NH 3 ‐ and NO −2 ‐oxidation respectively [Hynes and
Knowles, 1983]. Incomplete inhibition of nitrification by
ATU has previously been observed and attributed to the
resilience of some nitrifying archaea [Santoro et al., 2010].
However, there was no evidence of this in our study as
evidenced by the absence of NO−2 production in ATU treated
samples compared to the start of incubations. The vials were
sealed with rubber septa and incubated in the dark for
24 hours at 12°C. At the end of each incubation, the supernatant in each vial was filtered (0.7 mm, Whatman GF/F) and
the filtrate NO−2 concentration was determined by manual
colorimetric assay against six NaNO2 standards (Sigma;
>99.9% purity; standard range: 0.0–2.0 mmol L−1; R2>0.999)
[Grasshoff, 1983]. NH3 oxidation rates were calculated as
accumulation of NO−2 in the NaClO3 treatment compared
to the ATU treatment. The precision (0.3 mM NO−2 standard;
n = 3) and detection limit of NO−2 analysis were 5 nmol L−1
and 9 nmol L−1 respectively (NO−2 concentration in all samples was >10 nmol L−1). The corresponding limits of detection for rate calculations were 0.3 nmol L−1 h−1 in water and
0.2 nmol L−1 h−1 in sediments. The organic matter content of
the sediments (% LOI), determined by weight loss after
baking the vials at 350°C overnight, was 2.5 ± 0.2% (PS) and
1.7 ± 0.3% (ED) and did not differ between pH treatments.
2.2. Field Observations
[4] Sediment samples (muddy‐sand) for nitrification were
collected by diver in May 2008 from three sites (N1‐3) in
the vicinity of natural CO2 vents off the island of Ischia in
the Mediterranean Sea (40.73°N, 13.95°E). CO2 ebulition has
likely occurred at these sites for centuries as fluid seepage
(thermal springs) has been known on Ischia since Roman
times [Buchner, 1965]. Seawater pH at each of these sites was
8.2 (N1), 7.9 (N2) and 7.6 (N3), although advection of high‐
CO2 water causes substantial pH variability (± 0.2) at each
site [Hall‐Spencer et al., 2008]. NH3 oxidation rates were
determined as described above, except water from each of the
three Ischia sites was used to fill the glass vials.
3. Results
[5] Ammonia oxidation activity for Ischia samples, under
long‐term exposure to low pH, are shown alongside water
column and sediment data from the Plymouth Sound (PS) and
English Channel (ED) acidification experiments (Figure 1).
NH3 oxidation rates measured here were comparable to previously published data for coastal waters and sediments
[Carini et al., 2003; Henriksen et al., 1981; Jensen et al., 1996].
Average (±S.E.) water column NH3 oxidation rates at the
control pH were 2.4 ± 0.1 at PS and 3.1 ± 0.2 and 4.6 ± 0.5 nmol
L−1 h−1 at ED after 2 and 10 weeks. These rates were approximately 4‐ to 8‐fold higher than at Ischia (N1) at pH 8.2 (0.6 ±
0.2 nmol L−1 h−1). In the water column, NH3 oxidation generally decreased with decreasing pH, both in the long‐term
exposed Ischia samples and in the English Channel samples
incubated under different pH treatments. In both the PS and ED
experiments, NH3 oxidation rates in the water column declined
significantly with the reduction in pH (1‐way ANOVA;
p<0.01; all statistical tests incorporated the relative uncertainties of both NH3 oxidation rates and pH). At Ischia, whilst NH3
oxidation rates declined from N1 to N3, this decline was not
significant (1‐way ANOVA; p>0.1) (Figure 1). Differences in
water column NH3 oxidation rates for the two highest pH
treatments were only significant for ED after 10 weeks (T‐test;
p<0.05) and PS samples (T‐test; p<0.001).
[6] In sediments, there was no significant difference
between the mean NH3 oxidation rates under different pH
within the ED, PS mesocosms or at the Ischia site (1‐way
ANOVA; p>0.05). At the control pH, NH3 oxidation rates
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were 5–28 nmol L−1 h−1 ml−1 wet sediment at PS; 4–57 nmol
L−1 h−1 ml−1 wet sediment at ED and 97 ± 32 nmol L−1 h−1
ml−1 wet sediment at Ischia. Three cores from the 2‐week ED
experiment showed ∼3‐fold higher than average NH3 oxidation rates (189 ± 7 and 278 ± 3 nmol L−1 h−1 ml−1 wet sediment
at pH 8.0 and 206 ± 4 nmol L−1 h−1 ml−1 wet sediment pH 7.5).
Nevertheless, there was no significant difference between
mean NH3 oxidation rates under different pH treatments for
this experiment (1‐way ANOVA; p>0.05). Furthermore, mean
sediment NH3 oxidation rates for ED samples after 2‐ and
10‐weeks incubation at pH 8.0 were not significantly different (t‐test; p>0.05).
4. Discussion
4.1. Water Column NH3 Oxidation
[7] Our results confirm previous observations of low‐pH
inhibition of NH3 oxidation in the water column, but show no
evidence of such an effect in sediments. Furthermore, this
difference is consistent across three experiments with contrasting characteristics, suggesting that our conclusions are
widely applicable. Relatively few studies have focused on the
effect of ocean acidification (high CO2) on the physiology,
activity or community structure of marine microorganisms.
Pelagic mesocosm experiments have shown increased bacterial growth and protein metabolism under high CO2, but this
was thought to be an indirect response to changing phytoplankton dynamics (community structure and exudation of
organics) rather than a direct effect of high CO2 [Grossart
et al., 2006]. Here, CO2‐induced acidification of seawater
has been shown to have a pronounced and detrimental effect
on water column NH3 oxidation activity. In agreement with
previous work, we observed near‐complete inhibition of NH3
oxidation activity at pH 6.5 [Huesemann et al., 2002]. Yet,
other studies on single‐species cultures of Nitrosococcus
oceanus and Nitrosomonas europaea found that their activity
decreased, but remained detectable even at pH 5.5 and pH 5.4
respectively [Jones, 1992; Stein et al., 1997]. Importantly,
differences in NH3 oxidation rates between the two highest
pH treatments were only significant for PS (DpH = 0.2) and
ED sediments after 10 weeks of incubation (DpH = 0.4). This
shows that a small decrease in pH or short exposure to low pH
may not necessarily affect NH3 oxidation. A certain degree of
resilience to low pH may be expected, given seasonal pH
variability of up to 0.3 units in the western English Channel
(V. Kitidis et al., Seasonal dynamics of the carbonate system
in the western English Channel, submitted to Continental
Shelf Research, 2011). It has been suggested that the inhibitory effect of OA on NH3 oxidation may be due to substrate
(NH3) limitation of the ammonia monooxygenase enzyme, as
the NH3‐NH+4 equilibrium shifts towards the latter at low pH
[Huesemann et al., 2002; Stein et al., 1997; Suzuki et al., 1974].
Alternatively, the observed pH dependence of NH3 oxidation
activity in the water column may be related to changes in
microbial community structure. Such changes may result from
relative differences in susceptibility of different taxonomic
groups to low pH, though this remains speculative in the
absence of further information.
4.2. NH3 Oxidation in Sediments
[8] In contrast to the water column, acidification had no
significant effect on NH3 oxidation activity in surface sedi-
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ments. Substantial variability in the magnitude of sediment
NH3 oxidation rates was apparent between all PS and ED
sediments under each pH treatment. This variability may have
been caused by heterogeneity in organic matter content,
which has been shown to suppress NH3 oxidation activity in
lakes [Strauss and Lamberti, 2000]. However, we did not
observe a correlation between organic matter content (% LOI)
and nitrification rates here. Our data are apparently in contrast
with our earlier studies which attributed a decrease in nitrate‐
and concomitant increase in ammonia‐efflux from acidified
sediments to a decrease in nitrification activity [Widdicombe
et al., 2009; Widdicombe and Needham, 2007]. However,
direct measurements of nitrification were not performed
during these studies. Therefore, observed changes in nitrate
and ammonia efflux during previous work may reflect differences in other N‐cycling processes; dissimilatory nitrate
reduction and denitrification; or a reduction in nitrification
associated with the activity of macro fauna, which were
adversely affected by low pH. Both microbial diversity
[Laverock et al., 2010] and nitrification activity are enhanced
in the burrow walls of bioturbating fauna [Henriksen et al.,
1983; Welsh and Castadelli, 2004]. A decrease in nitrification may thus have occurred as a result of the deleterious
effect of OA on macro‐fauna during our previous work.
4.3. Potential Causes of Sediment/Water
Column Difference
[9] It is possible that pH within sediments differed substantially from our pH measurements, made in the overlying water,
However, this is unlikely given that only surface sediments (top
1 cm) were sampled here. The discrepancy between the effects
of OA on NH3 oxidation in the water column and in sediments
observed in our experiments may be explained by buffering of
the pH perturbation within sediments and/or by low‐pH adaptation of the sediment microbial community. This is a non‐
trivial distinction since pH buffering by sediments is a finite
process dependent on their mineral content, while microbial
adaptation would not cease under projected ocean acidification
over the coming century. Firstly, the pH perturbation may have
been buffered by alkalinity generation through the dissolution
of carbonate minerals, including calcite, Mg‐calcite and aragonite [Andersson et al., 2007]. Indeed, such alkalinity generation has been demonstrated for the PS sediments (H. Findlay
et al., manuscript in preparation, 2011). Nevertheless, the
experimental design maintained water pH at the nominal set
values for this experiment. It is therefore unlikely that alkalinity generation negated the high CO2 perturbation. Secondly,
the nitrifying microbial community present in sediments may
be adapted to occasional, low pH exposure. Although this
has not been shown in the marine environment, in soils there
is evidence for a switch from bacteria‐dominated to archaea‐
dominated nitrifying communities under acidic conditions
[Nicol et al., 2008]. Furthermore, the community composition
of nitrifying archaea inhabiting sediments has been shown
to be distinct from that within the water column [Francis
et al., 2005]. Given these differences in taxonomic composition between benthic and water column nitrifying communities, it is plausible that at least some benthic microorganisms
may have evolved to cope with low pH while their water
column counterparts do not. Following this argument, low‐pH
tolerant organisms may thereby be selected over time under
future OA. Thirdly, cell aggregation may be important in
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maintaining nitrifying activity in acidic soils as shown by the
reduction in the pH minimum of Nitrosomonas europaea
grown in sand columns compared to liquid culture [Allison
and Prosser, 1993].
4.4. NH3 Oxidation Under Long‐Term CO2 Exposure
[10] It is possible that community composition changes or
cell aggregation, may also take place under future ocean
acidification. If so, our experiments suggest that the magnitude
and function of benthic NH3 oxidation will remain unchanged.
To test this hypothesis, we have examined NH3 oxidation
activity in the water column and sediments off Ischia island,
where continuous, long‐term ebullition of thermogenic CO2 at
the seafloor provides a natural analogue for future ocean acidification from anthropogenic CO2 [Hall‐Spencer et al., 2008].
In agreement with our ED and PS experiments we observed a
decrease in mean water column NH3 oxidation with decreasing
pH for Ischia samples (70% reduction between pH 8.2 and
pH 7.6). However, this decrease was not statistically significant possibly due to low pH adaptation of the NH3 oxidizing
community (see above). Genetic adaptation or selection of the
microbial community is certainly a realistic possibility given
that fluid seepage (presumably including CO2) has been
taking place in this region since Roman times. In agreement
with our PS and ED sediment incubation experiments, we
found that low pH had no impact on sediment NH3 oxidation
(Figure 1). This agreement between mesocosm and in situ
data for such contrasting environments suggest that NH3
oxidation in sediments is unlikely to be affected either by
future ocean acidification or under an abrupt decrease in pH
as might be expected from leakage of sub‐sea floor stored
CO2. This has implications for modeling studies investigating
the impact of OA on marine ecosystems. For example,
Blackford and Gilbert [2007] predicted a 20% decrease in
pelagic nitrification by 2100. Our data suggest that a separate
parameterization of this effect is required for the benthic
component of such ecosystem models. Furthermore, we
highlight the need to identify the cause of NH3 oxidation
resilience to acidification in marine sediments, in order to
accurately predict the future response of this process.
5. Conclusions
[11] Our experiments have demonstrated that ocean acidification or CO2 leakage from sub‐sea floor carbon storage will
have a detrimental effect on water column ammonia oxidation
activity. Yet in sediments, this effect was absent, i.e., NH3
oxidation rates were not affected by low pH. This pattern is
repeated in samples collected from a natural analogue site
where sediments and seawater are exposed to long‐term (decades) CO2‐induced acidification. It is possible that the nitrifying
microbial community in sediments is to some extent adapted to
low pH or that pH buffering occurred. However, it remains
unclear how their function will respond to further environmental stress following exposure to low pH.
[12] Acknowledgments. This project was funded through the UK
Natural Environment Research Council (NERC) Oceans 2025 program.
B. Laverock was funded by a NERC algorithm studentship (NE/F008864/1).
[13] The Editor thanks Michael Beman and an anonymous reviewer for
their assistance in evaluating this paper.
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A. Beesley, D. Cummings, V. Kitidis, B. Laverock, L. C. McNeill, K. Tait,
and S. Widdicombe, Plymouth Marine Laboratory, Prospect Place, Plymouth
PL1 3DH, UK. ([email protected])
M. A. Osborn, Department of Biological Sciences, University of Hull,
Hull HU6 7RX, UK.
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