Enzymology and Ecology of the Nitrogen Cycle
Bioturbation: impact on the marine nitrogen cycle
Bonnie Laverock*†1 , Jack A. Gilbert*, Karen Tait*, A. Mark Osborn† and Steve Widdicombe*
*Plymouth Marine Laboratory, Prospect Place, Plymouth PL1 3DH, U.K., and †Department of Animal and Plant Sciences, The University of Sheffield, Western
Bank, Sheffield S10 2TN, U.K.
Abstract
Sediments play a key role in the marine nitrogen cycle and can act either as a source or a sink of
biologically available (fixed) nitrogen. This cycling is driven by a number of microbial remineralization
reactions, many of which occur across the oxic/anoxic interface near the sediment surface. The presence
and activity of large burrowing macrofauna (bioturbators) in the sediment can significantly affect these
microbial processes by altering the physicochemical properties of the sediment. For example, the building
and irrigation of burrows by bioturbators introduces fresh oxygenated water into deeper sediment layers
and allows the exchange of solutes between the sediment and water column. Burrows can effectively
extend the oxic/anoxic interface into deeper sediment layers, thus providing a unique environment for
nitrogen-cycling microbial communities. Recent studies have shown that the abundance and diversity of
micro-organisms can be far greater in burrow wall sediment than in the surrounding surface or subsurface
sediment; meanwhile, bioturbated sediment supports higher rates of coupled nitrification–denitrification
reactions and increased fluxes of ammonium to the water column. In the present paper we discuss the
potential for bioturbation to significantly affect marine nitrogen cycling, as well as the molecular techniques
used to study microbial nitrogen cycling communities and directions for future study.
Nitrogen cycling in marine sediments
Microbially driven cycling of nitrogen (Figure 1) in the
world’s oceans is a key process regulating biological
productivity. Sediments play a fundamental role in recycling
fixed nitrogen to the water column: it is estimated that
up to 80% of the nitrogen needed by primary producers
in shallow shelf seas is provided by benthic (sea floor)
remineralization reactions [1]. Conversely, marine sediments
also represent an important sink for fixed nitrogen via
the burial of organic matter; and by either the reduction
of nitrate into N2 or N2 O via denitrification; and/or the
conversion of nitrite and ammonium into N2 via anaerobic
ammonium oxidation (anammox) [2,3]. According to current
nitrogen budgets, benthic processes account for two-thirds
of the total marine conversion of fixed nitrogen into N2 :
300 Tg·year − 1 of a total 450 Tg·year − 1 [4]. Sediments are
therefore a key site for marine nitrogen cycling, because they
provide a largely anoxic environment in which anaerobic
reduction reactions, such as denitrification, can take place,
often within a few millimetres of the sediment/water interface
[3]. Sediments also provide a large repository for sinking
organic matter from the water column, with the fate of
this organic matter, once it reaches the sea floor, being
dependent upon the compartmentalization of the different
remineralization processes occurring within the sediment [5].
Once nitrogen within organic matter is remineralized through
ammonification, ammonium is then oxidized to nitrite and
Key words: bioturbation, microbial community structure, nitrogen cycle, nutrient flux,
oxic/anoxic interface.
Abbreviation used: SRB, sulfate-reducing bacteria.
1
To whom correspsondence should be addressed (email [email protected]).
Biochem. Soc. Trans. (2011) 39, 315–320; doi:10.1042/BST0390315
nitrate via nitrification. This occurs within the oxic zone
comprising a few millimetres at the sediment/water interface
(Figure 1). These oxidized compounds are then either released
to the water column or used to fuel reductive processes such as
denitrification. Thus nitrification performs several important
functions, linking (i) the oxic and anoxic reactions within the
nitrogen cycle, (ii) the production of new compounds to the
loss of fixed nitrogen, and (iii) the decomposition of organic
matter to the release of nutrients from the sediment [2,3,6].
For this reason, the oxic/anoxic interface occurring at the
sediment surface is of particular importance in the marine
nitrogen cycle [3].
Investigating the marine nitrogen cycle
Despite its obvious importance, our understanding of the
marine nitrogen cycle is far from complete. In particular, our
knowledge concerning the identity, distribution and function
of the key microbial organisms involved is rapidly evolving.
For example, the recent discoveries of both anaerobic
ammonium oxidation (anammox) and of archaea as key
drivers of ammonia oxidation have sparked considerable
research effort into the distribution and importance of these
processes in the marine realm. These discoveries have been
reviewed extensively elsewhere [7–9]. However, controversy
remains over the comparative importance of denitrification
and anammox, especially within the oxygen minimum
zones of the world’s oceans [10]. Much of this research
has relied on the application of genetic markers to study
the micro-organisms responsible for the different nitrogen
cycling processes (Table 1) combined with isotope-pairing
techniques [11] to study rates of nitrification, denitrification
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Biochemical Society Transactions (2011) Volume 39, part 1
Figure 1 The marine nitrogen cycle occurring across oxic/anoxic interfaces
Unshaded boxes indicate organic nitrogen. PON, particulate organic nitrogen. DON, dissolved organic nitrogen. Shaded
boxes indicate dissolved inorganic nitrogen. Processes: A, nitrogen fixation; B, ammonification; C, ammonia oxidation;
D, nitrite oxidation (C+D = nitrification); E, nitrate reduction; F, nitrite reduction (E+F = denitrification); G, dissimilatory
reduction of nitrite to ammonium (DNRA); H, anaerobic ammonium oxidation (anammox). Broken arrows indicate fluxes
in/out of sediment porewater; continunous arrows indicate microbial remineralization reactions. Arrowhead sizes across the
sediment/water interface reflect the predominant flux direction in coastal sediments. NO (Nitric oxide) and N2 O (nitrous
oxide) are intermediate products of both ammonia oxidation (C) and nitrite reduction (F).
and anammox. These, combined with the advent of highthroughput sequencing technologies, are allowing us to
explore more fully the marine nitrogen cycle in order to
address many of the current knowledge gaps.
Bioturbation: an introduction
Macrofauna living in or on marine sediments can significantly
alter both the physical structure and chemical composition
of the sediment through their burrowing and irrigation
activities. For this reason, they have long been considered
‘ecosystem engineers’ [21], and their presence can create
unique microniches for sediment micro-organisms to inhabit
[22–24]. To date, most bioturbation studies have concentrated
on burrowers such as polychaete worms and crustaceans (e.g.
[25–29]). However, bioturbation may be carried out by other
benthic macrofauna, including molluscs and echinoderms,
as well as pelagic bottom-feeders such as walrus, fish and
stingrays, and meiofaunal communities such as larvae
and nematode worms [30].
Infaunal tubes and burrows are semi-permanent or
permanent structures that differ in size, appearance and
composition according to the mode of life and habits of
the inhabitant. A previous study has calculated the global
volume of bioturbated sediment to be >20 700 km3 (based
on an estimated ocean surface area of 360 million km2 ) [31];
clearly, the sheer abundance of these ‘ecosystem engineers’
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on a substantial proportion of the world’s shallow shelf
marine habitats via their bioturbating activities. It has long
been known that the macrofaunal burrow environment can
support different physicochemical properties from those
experienced in both the sediment surface and the surrounding
ambient sediment [32,33]. In particular, the burrow may
be frequently or intermittently ventilated by its inhabitant,
thereby introducing fresh oxygenated water into the burrow;
allowing greater solute exchange and an extension of
the oxic/anoxic interface into deeper sediment [5,34]. For
example, it is estimated that the presence of thalassinidean
shrimp burrows can increase the sediment surface area by up
to nine times [35]. Additionally, it is thought that the physical
mixing of sediment during burrow building and maintenance
activities can contribute to increased biodiversity of both
meiofaunal [36] and microbial communities [29,37].
Microbial community structure within
sediment burrows
The layer of sediment, organic matter and biopolymers that
make up the burrow wall has the potential to affect the benthic
nitrogen cycle. First, bacterial abundance and activity can be
10-fold higher in the macrofaunal burrow wall compared with
surrounding sediment [27,32]. Secondly, the composition
of the microbial communities inhabiting burrow walls can
Enzymology and Ecology of the Nitrogen Cycle
Table 1 Genetic markers for nitrogen-cycling processes showing genes for which probes or PCR primers have been developed
Based on data taken from [12] (and references therein). AOB, ammonia-oxidizing bacteria.
Transformation
Micro-organisms
(principally) responsible
Gene(s)
Protein
N2 fixation
nifHDK
Nitrogenase
Diazotrophs
Nitrite assimilation
Nitrate assimilation
nirB
narB, nasA
Nitrite reductase
Assimilatory nitrate
reductase
–
Nitrate reduction and
denitrification
narG (membrane bound) napA (periplasmic)
nirS, nirK
norB
Nitrate reductase
Nitrite reductase
Nitric oxide reductase
Genes are widespread across
Bacteria, Archaea and
Eukarya
[13]
nosZ
Nitrous oxide
reductase
Nitrite reductase
Bacteroides spp.,
[13,14]
Ammonia
Planctomycetales and
Proteobacteria
Nitrosomonas, Nitrospira,
[15–17]
Dissimilatory nitrate
reduction to
ammonia (DNRA)
Ammonia oxidation
nrf (nrfA)
amo (amoA)
mono-oxygenase
Nitrite oxidation
nxrB
Nitrite oxidoreductase
Anammox
?hao? (also found within groups of nitrifiers)
Planctomycete-specific 16S genes
Hydroxylamine
oxidoreductase
also be significantly different from those in the surrounding
sediment, in terms of both their structure and diversity
[28,29,38]. More specifically, Satoh et al. [39] found that
the ammonia-oxidizing and nitrite-oxidizing communities
in the burrow walls of a polychaete worm were similar
to those in surface sediment and the abundance of gene
markers for these functional guilds was much higher in the
burrow wall than in the bulk sediment. However, it should
be noted that the exact effects of bioturbation on microbial
community structure may be dependent upon the individual
burrow builder. For example, the burrows of specific nereidid
worms [40], thalassinidean shrimp [27] and fiddler crabs
[28] were found to be more similar to the surrounding
subsurface (anoxic) sediment than to surface sediment in
terms of microbial community structure. Conversely, the
burrows of some polychaete worms [38] and thalassinidean
shrimp [28,29] were found to contain microbial communities
more similar to those in the oxygenated surface sediment than
those in subsurface ambient sediment. It is therefore probable
that the individual burrowing and irrigation behaviours of
different macrofaunal burrowers contribute to creating a
physicochemical environment that may in itself be unique,
but more similar to either the surface or subsurface sediment,
depending on the burrow inhabitant [23,32].
Influence of bioturbation on nutrient
fluxes and nitrogen cycling rates
Nutrient flux rates depend on many factors, including the
type of sediment substrate and the mode and extent of
Reference(s)
(AOB in the
β-Proteobacteria
subgroup) and
Thaumarchaeota (Archaea)
Nitrobacter and Nitrospira
[18]
Planctomycetes
[19,20]
bioturbation. Burrow walls effectively act as an extension
of the oxic surface of the sediment, which has particular
relevance to nitrification–denitrification reactions coupled
across the oxic/anoxic interface [41]. Fluxes of O2 ,
total CO2 and dissolved inorganic nitrogen across the
sediment/water interface have been observed to increase by
2.5–3.5 times in bioturbated sediment relative to control nonbioturbated sediment [5,26,42]. The concentration profiles
for ammonium, nitrite and nitrate are linked with changes
in oxygen concentration. Nedwell and Walker [43] showed
that the presence of amphipods in Antarctic sediments
doubled the production of NH4 + by direct release or
stimulation of vertical transport processes, and Aller and
Aller [44] demonstrated that the net remineralization rate for
NH4 + increases as the efficiency of solute exchange with the
overlying water increases. Meanwhile, several studies have
shown that bioturbation activity increases denitrification by
up to 400% [26,45,46]. However, this is not simply a direct
consequence of macrofaunal bioturbation, rather the result
of environmental alterations which affect microbially driven
biogeochemical processes. For instance, Howe et al. [26]
noted that most of the increase in denitrification stimulated by
the presence of burrowing shrimp was fuelled by nitrification
occurring within the burrow walls, suggesting that it is the
elevated rates of nitrifying bacteria utilizing the increased
fluxes of O2 and NH4 + , rather than the direct supply of
NO3 − , that is the driving factor. It is generally accepted
that the most important role of bioturbation in stimulating
remineralization reactions, such as denitrification, is the
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introduction of oxygen into subsurface sediments which
can stimulate the decay of organic matter by a factor of
ten [23].
The impact of bioturbation on microbial activity is
complicated further by the existence of microniches within
sediment systems and within the burrow wall in particular
[28]. The burrow can be viewed as a unique environment
which experiences fluctuations in its biogeochemistry as
a result of the irrigation, burrow building and burrow
maintenance behaviours of its inhabitant; this may indeed
lead to unique communities of micro-organisms inhabiting
the burrow wall [23]. Burrow walls are therefore not
geochemically uniform structures, and often exhibit patterns
of zonation and heterogeneity [5]. For example, nitrogen
fixation is normally assumed to be unimportant in burrows
because of the high levels of oxygen and ammonium, both
of which inhibit the activity of the nitrogenase enzyme.
However, Bertics et al. [24] observed far greater levels of
nitrogenase activity in sediments that were heavily populated
by burrowing ghost shrimp. This activity was apparently
linked to the presence of nifH genes (Table 1) in SRB
(sulfate-reducing bacteria), suggesting that the SRB were able
to exploit anoxic microniches within the shrimp burrows,
and contribute to increased benthic nitrogen fixation and
sulfate reduction. The authors suggest that in benthic nitrogen
cycling models, bioturbated sediments could be a source
of fixed nitrogen as well as a loss term due to stimulated
denitrification [24].
A greater understanding of the occurrence and activity of
these microbial microniches could significantly change our
understanding of the effects of bioturbation on the marine
nitrogen cycle. This may be particularly important when
we consider that the changes in sediment biogeochemistry
and microbial diversity brought about by bioturbation may
have indirect effects on the nitrogen cycle via changes to the
anaerobic respiration pathways that occur in sediments. For
example, any increase in sulfate reduction is likely to have
an inhibitive effect on both nitrification and denitrification
in the burrow [47]. Meanwhile, it appears that within
fiddler crab burrows in salt marsh sediments, iron-reducing
bacteria may out-compete SRB [48]. This repartitioning
of remineralization reactions could be important because
the inhibitory effects of sulfide on nitrification may be
ameliorated by increased amounts of iron(III) present
in the burrow wall, which rapidly scavenges sulfide from
the environment [23,49]. The spatial overlap of respiration
processes, including denitrification, sulfate reduction and
iron reduction, may therefore be encouraged by the presence
of burrow microniches [23,24,50].
Challenges and future directions
We are still at the beginning of our understanding of how
bioturbating macro-organisms interact with the sediment and
its microbial communities, and the effects this interaction
has on important biogeochemical cycles in the marine
realm. It is clear from the numerous studies on nutrient
flux measurements and biogeochemical rates that microbial
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Several studies (as cited previously) have also shown that
microbial diversity and abundance may be greater in
burrow walls, which may also contain a different microbial
community from that of the surrounding sediment. However,
it is important now to investigate more deeply the taxonomy
and functional diversity of burrow communities, specifically
in relation to the abundance and activity of key nitrogen
cycling genes.
Sampling marine sediments is challenging, especially when
it is important to retain as much as possible the in situ
biogeochemical conditions of the sediment. Many studies
have sampled in situ infaunal burrows, mostly at periods
when they are exposed by low tides (e.g. [28]). Some have also
used mesocosms to investigate the burrow in the laboratory
environment (e.g. [29]), whereas others have used ‘mimic’
burrow structures in the laboratory (e.g. [51]). All of these
techniques have their attendant benefits and drawbacks, and
often the choice will be down to logistical questions as
well as knowledge of which technique will allow the most
effective sampling for the analyses to be done. However, it
is important to note that mesocosm studies will inevitably
differ from those conducted in situ [23,52], and, where
possible, it is essential to take into account the changes in
macrofaunal and microbial activity that occur with season,
temperature, salinity, sediment type and organic loading,
and to compare any laboratory results with relevant in situ
data.
Finally, given the clear relationship between bioturbating
activity and microbial nutrient cycling, it would be beneficial
to consider the factors that may affect this relationship.
In particular, it is known that many bioturbators may be
physiologically and/or behaviourally sensitive to environmental changes such as increasing seawater temperature
and decreasing pH (e.g. [53–55]). In addition, it seems that
there is increasing eutrophication within coastal waters from
industrial and agricultural run-off [4], and an expansion
of the world’s oceans’ oxygen minimum zones, which are
themselves important sites for pelagic denitrification and
anammox [56]. Considering the relatively rapid changes that
are occurring within our oceans, a key question should be
what knock-on effects these changes will have on macrofaunal
bioturbator behaviour, and hence on the essential functioning
of nitrogen cycling micro-organisms in the sediment.
Funding
B.L. acknowledges funding from a Natural Environment Research
Council (NERC) algorithm Ph.D. Studentship [NE/F008864/1] and
from the NERC-funded programme Oceans 2025 (Theme 3: Coastal
and Shelf Processes).
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Received 29 October 2010
doi:10.1042/BST0390315