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Microb Ecol
DOI 10.1007/s00248-008-9421-8
REVIEW ARTICLE
Conceptual Bases for Prey Biorecognition and Feeding
Selectivity in the Microplanktonic Marine Phagotroph
Oxyrrhis marina
Claire M. Martel
Received: 13 April 2008 / Accepted: 19 June 2008
# Springer Science + Business Media, LLC 2008
Abstract It is suspected that phagotrophic marine protozoa
might possess feeding receptors that enable them to discern
the nutritional quality of individual prey items (during preyhandling) on the basis of their cell-surface biochemistry.
This article reviews advances in our understanding of the
molecular mechanisms that mediate the biorecognition and
selection of nonself (microalgal) prey items by the microplanktonic marine phagotroph Oxyrrhis marina. The
potential importance of lectin–glycan interactions is first
considered in view of findings which demonstrate that O.
marina possesses lectin-like feeding receptors specific for
prey-surface (mannose) glycoconjugates. Secondly, some
conceptual bases for indirect or ‘opsonic’ modes of prey
biorecognition mediated by soluble prey-labelling proteins
are presented. Finally, the possibility that some accounts of
selective feeding in O. marina might result from the
noxious effects of prey-associated chemicals rather than
active ‘distaste’ by phagotrophic cells is discussed. Recent
evidence for toxic superoxide (O2−) production by marine
microalgae is afforded particular attention given that release
of O2− anions can be exacerbated by the binding of
mannose-specific lectins to the microalgal cell wall; a novel
model for grazing-activated chemical defence is proposed.
Introduction
Phagotrophic marine protozoa ingest bacteria, phytoplankton, other protozoa, metazoan eggs and even small
crustacea. In this way, they influence food-web structure
C. M. Martel (*)
Institute of Life Science, School of Medicine, Swansea University,
Singleton Park SA2 8PP, UK
e-mail: [email protected]
and succession [29], and biogeochemical cycling within
aquatic environments [58]. Since the formal recognition of
aquatic ‘microbial loop’ communities [50], there has been
sustained interest in the feeding preferences of marine (and
freshwater) protozoa; far from being indiscriminate grazers,
many species of protozoa show highly specific or ‘selective’
ingestion behaviours [7, 19, 36, 55, 58]. For clarification, it
is generally understood that selective feeding has occurred
when (during/after grazing) there results an imbalance
between the proportion of prey types in the diet of predatory
cells and the proportion of the same prey types in the
environment [11].
The influence of passive, morphological factors (e.g.,
prey size) on the outcome of microbial predator–prey
interactions is well acknowledged; there is a wealth of
evidence for size-selective ingestion in the literature [12,
23, 42, 61]. Prey cell shape and motility also influence
predator ingestion behaviour; some protozoa simply cannot
consume complex (e.g., filamentous) prey growth forms
[28]; highly motile prey can avoid or escape ingestion [21,
40, 67]. Importantly, some prey items might appear to be
rejected or ‘selected against’ because they are too big, too
small or simply too motile for predatory cells to capture and
ingest.
It has long been suspected that some protozoa might
possess feeding receptors (e.g., contact chemoreceptors
[71]) which enable them to judge the profitability of
different prey items on the basis of their cell-surface
biochemical composition. Given that changes in the cellsurface biochemistry and toxicity of marine microalgae
occur when they are nutrient stressed or nutrient imbalanced [2, 26, 37], the ability to detect these changes would
be advantageous for predatory species. However, until
recently, speculation regarding the potential for chemical
recognition processes between predatory and prey cells has
C. M. Martel
tended to focus on the signal potential of soluble chemical
species. The importance of prey-associated chemical compounds which deter predator grazing is a recurrent theme in
marine literature [65, 73–75].
This review revisits reports of selective feeding in the
phagotrophic marine protozoan Oxyrrhis marina in light of
an accumulation of evidence which suggests specific,
receptor-mediated mechanisms facilitate the adhesion and
biorecognition of individual prey items by certain species
of protozoa [59, 69, 70, 78]. A study which reports that O.
marina uses lectin-like feeding receptors to recognise
carbohydrate moieties on potential prey items [78] has
been afforded particular attention. Importantly, carbohydrate moieties are natural cell-surface and structural
components of microalgal and bacterial prey items in the
marine environment [5, 31, 51]; it is entirely possible that
they are implicated in the process of prey biorecognition by
O. marina. Some conceptual bases for indirect modes of
prey biorecognition mediated by soluble prey-labelling
proteins are also discussed. To conclude, a recent review
of superoxide (O2−) production in marine microalgae [35] is
considered alongside evidence that O2−-release from microalgae can be stimulated by lectin-binding [47]. A novel
model for grazing-activated chemical defence in superoxideproducing marine microalgae is proposed.
Phagocytosis and Phagotrophy
The capacity for phagocytosis or ‘cell eating’ is demonstrated by a diverse range of cell types including mammalian macrophages [48, 49], free-living amoeba [3], and
planktonic marine protozoa [58]. In mammals, the phagocytosis of foreign items by professional phagocytes (e.g.,
macrophages, dendritic cells and neutrophils) results in
immune protection for an individual [46]; in protozoan
predators, it can be a facultative or obligate mode of
nutrition [27]. Despite dissimilarities in the context of
phagocytosis, the factors that influence initial biorecognition and adhesion events between nonself particles and
phagocytic cells [64] are potentially universal. For all
phagocytic cell types, the ability to identify nonself
particles is essential, particularly if the engulfment of toxic
or unsuitable or targets is to be avoided.
Nonspecific Physiochemical Interactions
Cellular interactions between phagocytic and prey cells are
subject to forces similar to those which determine colloidal
aggregation between surfaces [41]. Adhesion depends on
the balance of electrostatic and hydrophobic interactions
between particles/cells. Due to the glycoproteins and
mucopolysaccharides of their glycocalyx, cell surfaces are
negatively charged; thus the electrostatic effects between
them are repulsive [53]. Conversely, the influence of
hydrophobic forces (determined by the ratio of hydrophilic
and hydrophobic cell-surface components) are strongly
attractive [25]. It has been widely demonstrated that
phagocytic cells tend towards engulfing particles whose
surface hydrophobicity is greater than their own [10, 39, 41,
43, 72]. However, in the field of marine microbiology,
debate surrounds the potential that subtle variations in prey
surface hydrophobicity and charge might affect the ingestion rates and predation behaviour of phagotrophic protozoa. Monger et al. [43] propose that the rate at which
marine bacteria are cleared from suspension by phagotrophic
protozoa could vary by as much as twofold due solely to
natural variation in cell surface hydrophobicity. In contrast,
Matz and Jürgens [39] argue that variability in bacterial cell
hydrophobicity and cell-surface charge is not adequate to
influence rates of prey uptake or prey selection by predatory
cells. This disagreement is important given that the cellsurface biochemistry (and thus electrostatic properties) of
microalgae differs with their nutrient status. Given that
nutrient-deficient microalgae are abundant in cell-surface
glycoconjugates [2, 32, 37], it might be that enhanced
production of prey-surface glycoconjugates accentuates the
strength of repulsive (negative–negative) electrostatic forces
at the cell–cell interface between predatory and prey cells.
However, a few attempts have been made to address this
possibility.
Interestingly, the importance of particle- and cell-surface
charge for defensive, immunological processes in metazoa
is well-documented. Positively charged foreign particles
elicit more vigorous encapsulation responses in marine
bivalves and other invertebrates [77]. It has been reported
that the success of some parasitic and pathogenic cells is
linked to their electrostatic properties; those with a strong
negative surface-charge are more able to avoid host
immune responses [14]. In humans, electrostatic forces are
involved in antibody–antigen interactions of the major
histocompatibility complex [44]. Furthermore, synergistic
interactions between nonspecific electrostatic forces and
more specific receptor–ligand mechanisms add layers of
complexity to the cellular mechanisms that regulate innate
immunity [14, 30]. These considerations imply that more
rigorous investigation of the influence of electrostatic forces
on the outcome of feeding interactions between phagotrophic
protozoa and individual prey items is required.
Specific Receptor–Ligand Interactions
In mammalian organisms, numerous receptor-based recognition mechanisms mediate cellular recognition processes
[9]. One group of receptors implicated in cell–cell
interactions are lectins—carbohydrate-binding proteins that
Prey Biorecognition and Feeding in Oxyrrhis marina
able to ‘taste’ potential prey items during the prey handling
phase of predator–prey interactions.
Biorecognition of Poor Quality Prey
Figure 1 Receptor-mediated prey recognition. Predator feeding
receptors might interact with specific prey-surface biorecognition
molecules (e.g., mannose moieties [78]). Note that good quality (e.g.,
nitrogen-sufficient) microalgae A produce fewer cell-surface mannose
moieties than B nitrogen-stressed, and C nitrogen-limited (poor
quality) microalgae [37]
agglutinate cells [34]. Some classes of lectin function at the
cell surface, facilitating agglutination, attachment and
adhesion; others underpin intracellular recognition processes [18]. Of notable importance is evidence for lectinmediated phagocytosis or ‘lectinophagocytosis’ during
which lectins on the surface of a phagocytic cell combine
with complementary sugars on the surface of the target
particle in a lock-and-key manner [56]. In mammals,
lectinophagocytosis mediated by the transmembrane macrophage mannose receptor is particularly well-documented
because it plays a fundamental role in innate immunity [56,
57, 63]. In the field of marine research, lectin–glycan
interactions mediate the obligate and highly specific
relationship between symbiotic dinoflagellates and reef
building corals [76]. Furthermore, a mannose-rich cell wall
glycoprotein on the red microalga Porphyridium sp. is
believed to be a biorecognition site for its specialist
predator—a Crypthecodinuim cohnii-like dinoflagellate
[59, 69, 70]. Evidence for lectinophagocytosis has been
reported in cell types from estuarine and marine organisms
(metazoa and protozoa) including seabream leucocytes
[52], catfish leucocytes [1], and most recently, the microplanktonic marine phagotroph O. marina [78]. The latter
study reports that lectin-like predator feeding receptors
specific for prey-surface mannose residues facilitate prey
adhesion and biorecognition by O. marina.
Given the specificity of many lectin–glycan interactions
[34], hypotheses which implicate the potential importance
of lectin–carbohydrate interactions for prey selection by O.
marina (and other phagotrophic protozoa) are conceptually
feasible (Fig. 1). It might be that phagotrophic cells possess
a range of lectin-like feeding receptors (with different sugar
specificities) that enable them to sort between prey items of
differing nutritional quality on the basis of their cell-surface
carbohydrate composition. Phagotrophic cells may thus be
A recurrent example of feeding selectivity in O. marina is
its ability to discriminate against the prymnesiophyte
microalga Isochrysis galbana in mixed prey experiments
[19, 23, 36]. The ‘distaste’ that O. marina shows towards I.
galbana is interesting because it is usually associated with
nitrogen-stress (an elevated C:N ratio) in the phototroph
[19, 36]. Nitrogen-stress is known to result in enhanced
polysaccharide production in numerous marine microalgae
[2, 32]; moreover, it has recently been shown [37] that
nitrogen-limited I. galbana are more abundant in mannoselinked cell-surface glycoconjugates than nitrogen-sufficient
(Fig. 1). This result is interesting: because O. marina
possesses mannose-specific receptors [78], it might be
reasoned that mannose-rich, nitrogen-limited (i.e., nutritionally poor quality) I. galbana should be adhered to and
ingested more readily. However, this is not the case;
experiments with O. marina have shown that nitrogendeficient I. galbana are ingested at lower rates than
nitrogen-sufficient [19, 23, 36].
In the case of O. marina, it is possible that lectin–glycan
interactions may facilitate adhesion to potential prey items
but that alternative and/or additional receptors specific for
prey-surface ‘eat me’ or ‘don’t eat me’ molecules may
mediate phagotrophy (Fig. 2). Certain prey species may
display cell-surface predator deterrents which inhibit or
counter the adhesion mediated by lectin–glycan interactions
(Fig. 2a). Such prey-ingestion and/or prey-rejection signals
may be of carbohydrate origin or of a completely different
chemical nature. Alternatively, given the complexity and
Figure 2 Potential mechanisms for the biorecognition of poor quality
(e.g., nitrogen-limited) microalgae. A Predatory cells might recognise
specific prey-surface ‘don’t eat me’ molecules. Alternatively, biorecognition molecules (e.g., prey-surface glycoconjugates [78]) on
poor quality microalgae may differ in their structure, isotopic
composition or orientation (B). Finally, compounds lost from
nitrogen-limited prey (e.g., mucopolysaccharides [2]) might impair
the efficiency of predator feeding receptors (C)
C. M. Martel
enhanced production of poly- and mucopolysaccharides
occurs in nitrogen-stressed microalgae in the absence of
predation pressure [37]. Carbohydrates are metabolised to
sequester excess carbon/photosynthates when the growth
and proliferation of microalgal cells is limited by nitrogenstress. In this respect, the negative/inhibitory effect of any
carbohydrates lost from microalgae on prey biorecognition
mechanisms/protozoan feeding receptors (Figs. 2c, 3c and
4d) should not be regarded as an algal defence strategy but,
perhaps, a fortunate consequence of microalgal physiology.
Figure 3 Potential mechanism of action for soluble prey-labelling
proteins. Predatory cells might coat potential prey items with labelling
proteins specific for prey-surface biorecognition molecules [54]. A
Labelling proteins may adhere readily to good quality (e.g., nitrogensufficient) prey. Conversely, the structure, orientation, isotopic
composition or density of biorecognition molecules on poor quality
prey (B) may prevent binding. Binding could also be inhibited by
prey-surface biochemical components (C) and/or exudates that
originate from certain prey species
specificity of many receptor-mediated (including lectinmediated) processes, it may be that the predator feeding
receptors reported by Wootton et al. [78] cannot interact
with certain chemical species on poor quality prey.
Variation in the structure, isotopic composition and/or
orientation of prey-surface (e.g., carbohydrate) biorecognition molecules on nutrient-deficient prey might affect the
efficiency of phagocytosis (Fig. 2b). It might also be that
dissolved compounds lost from some algal prey items (e.g.,
mucopolysaccharides [2]) could impair the efficiency of
prey biorecognition by competing at the active site of
predator feeding receptors (Fig. 3). It should be noted that
Figure 4 Chemical inhibition of predator feeding receptors and
soluble prey-labelling proteins. A Prey-associated chemical compounds might block or alter the active sites of any predator-feeding
receptors. B Bioaccumulated (or bound) chemicals could act on
internal receptor domains and/or inhibit signal transduction pathways
associated with prey biorecognition. C Chemicals could block the
Soluble Prey-Labelling Proteins
Consideration of immunological literature [e.g. 24, 33, 68]
raises the possibility that ‘opsonic’ mechanisms may be
involved in the process of prey biorecognition by O.
marina (and other protozoa). Opsonins are serum components that function as a bridge between microorganisms
and the professional phagocytes that effect immune
responses in mammals. Of particular interest are collectins
(e.g., Holmskov et al. [24]), a class of serum proteins that
interact with complementary carbohydrates on microorganisms and specialised collectin receptors on phagocytic cells.
The relevance of opsonic phagocytosis to the study of
microbial feeding interactions is highlighted by a study of
prey recognition, capture and phagocytosis by the phagotrophic protozoan Actinophrys sol. [54]. This research paper
identifies a glycoprotein (gp40) stored in secretory extrusomes of predatory cells. When a prey cell contacts the
surface of Actinophrys, adhesive gp40 molecules are
discharged; these adhere to the surface of the prey item
production of prey-labelling proteins or inhibit protein binding. D
Noxious compounds and/or mucopolysaccharides lost from certain
prey could create a near-field chemical environment that inhibits prey
biorecognition mediated by predator feeding-receptors and/or soluble
prey-labelling proteins
Prey Biorecognition and Feeding in Oxyrrhis marina
which Actinophrys then recognises as nonself and proceeds
to phagocytose. Of interest is the suggestion that binding of
gp40 to the surface of target (prey) cells initiates their
phagocytosis in a manner which parallels the phagocytic
pathways mediated by opsonic serum proteins in mammalian organisms [54].
It might be that similar opsonic or ‘prey-labelling’
mechanism/s mediate prey biorecognition and/or prey
targetting in O. marina (Fig. 3). On a conceptual level,
the binding efficiency of any soluble prey-labelling proteins
could be affected by any changes in prey surface
biochemistry that are associated with different nutrient
regimes [2, 32, 37]. For example, soluble prey-labelling
proteins may readily adhere to biorecognition markers on
good quality (e.g., nitrogen-sufficient) prey items (Fig. 3a).
Conversely, the structure, orientation, isotopic composition
or density of biorecognition molecules on poor quality prey
might inhibit or prevent binding (Fig. 3b). Prey-surface
biochemical components and/or exudates that originate
from certain (e.g., poor quality) prey might also inhibit
the binding efficiency of prey-labelling proteins (Fig. 3c).
Culture Preconditioning and Prey Selection
The conceptual bases for direct and indirect modes of prey
biorecognition mediated by (1) predator-surface feeding
receptors and/or (2) soluble prey-labelling proteins are
interesting. However, they are not adequate to explain how
or why phagotrophic protozoa such as O. marina cease to
feed on certain prey items following a period of culture
preconditioning with them [6, 19, 36]. For example, the
‘distaste’ that O. marina shows towards nitrogen-limited I.
galbana is heightened in predatory cells that have recently
ingested the phytoflagellate [19, 36]; O. marina appears to
‘learn’ not to ingest I. galbana cells that are of poor
nutritional quality. It has already been postulated that
chemical discrimination of poor quality prey items by
predatory cells may involve the turnover of specific
recognition systems that are synthesised following the
exposure of predatory cells to certain prey items [19]. An
alternative hypothesis—that existing recognition systems
might be repressed or derepressed such that some prey
items (or specific prey-surface biochemical markers) can be
‘deselected’ or ‘selected’ by predatory cells—has also been
proposed [19]. The former mechanism could be important
for predatory species that ingest prey items that become
noxious/unpalatable (e.g., under nutrient imbalanced conditions) or when predatory cells graze mixed-prey assemblages. It constitutes a sort of biochemical memory that
might enable predatory cells to sort between poor and good
quality food items from the same (or different) prey species.
The latter system could constitute a biochemical basis for
self- and nonself recognition and, consequently, might
regulate cannibalistic behaviour within predatory populations.
It follows that cannibalistic ingestion observed in O.
marina populations [15, 19, 38, 66] may only be enabled
(prey-recognition systems are repressed) when no suitable
nonself prey items are available for consumption. When
suitable nonself prey are available, molecular-level self
and nonself recognition mechanisms might be derepressed
to ensure that conspecifics are not ingested. Interestingly,
cell-surface galactosamine moieties (potential self-recognition
molecules) have been identified on O. marina but not I.
galbana [51]. Furthermore, haemagglutination experiments [78] have shown that O. marina possesses
galactosamine-binding proteins (agglutination/lectin activity was inhibited by galactosamine). However, the function of these carbohydrate moieties and binding proteins
(e.g., self-recognition) remains to be determined. It is
tempting to speculate about the potential for self- and
nonself recognition mechanisms; however, there may not
be any molecular-level controls on cannibalistic ingestion
in O. marina. A recent study [38] which highlights the
importance of morphological controls (the size and
motility of conspecifics) on cannibalism in O. marina
populations underscores this consideration.
It is noteworthy that the efficiency and action of any
molecular-level prey recognition mechanisms are likely to
be affected by the nutritional status (and thus preculture
diet) and/or age of predatory cells. Firstly, any recognition
systems that operate in nutrient-sufficient O. marina might
be degraded (or not synthesised at all) in nutrient-deficient
cells. Secondly, if a ‘biochemical memory’ does condition
the ingestion preferences of phagotrophic cells, its longevity
may be linked to the cell cycle; recently divided cells might
not continue to synthesise specific prey recognition systems
[19] because their biochemical memory has been erased or
reset through cell division. These considerations could
explain evidence for unselective feeding in O. marina. For
example, in a recent study of prey (I. galbana) location,
recognition and ingestion by O. marina, vacuoles deplete
(containing no I. galbana food vacuoles) O. marinaingested I. galbana indiscriminately [36]. This may have
been because the vacuole that deplete cells used in
experimental work had recycled any cell-surface macromolecules that were needed for prey biorecognition or
because they were from younger (recently divided) generations that had never been exposed to the I. galbana
preculture diet. It is also possible that any nitrogenous,
protein-linked receptors involved in refined prey recognition and ingestion behaviour may be degraded (or not
synthesised at all) in nutrient-stressed (vacuole deplete) O.
marina populations wherein the need to conserve intracellular nitrogen reserves for more essential cellular processes,
predominates over the need to feed selectively.
C. M. Martel
Chemically Mediated Predator–Prey Interactions
H. akashiwo toxicity. Unlike phagotrophic protozoa that
engulf whole prey items, A. longum is effectively able to
sample H. akashiwo and thus may cease to feed on the
toxic raphidophyte long before bioaccumulated toxins exert
their full effect.
Given evidence for grazing-activated chemical defence
between protozoan grazers and marine microalgae [e.g.,
73–75], the possibility that the discrimination shown
towards certain prey species results from the action of
noxious prey-associated compounds (rather than active
‘distaste’ on the part of predatory cells) warrants consideration. It might be that some prey-associated compounds are
able to inhibit any receptor-mediated and/or prey-labelling
mechanisms that are involved in the process of prey
biorecognition by phagotrophic protozoa (Fig. 4). Firstly,
chemical compounds exuded or lost from certain prey
species might block or alter the active sites of any predator
feeding receptors (Fig. 4a). Secondly, chemicals bioaccumulated from ingested prey items could act on internal
membrane domains and/or inhibit signal transduction pathways associated with prey biorecognition (Fig. 4b). It is
already suspected that the ingestion preferences of some
protozoa are influenced by their ability to tolerate certain
prey-associated chemicals [13, 65]. Furthermore, there is
evidence to suggest that such chemical tolerance limits are
highly species-specific. For example, exposure to lipophilic
toxins from the marine microalga Karlodinium micrum
causes cell-membrane lysis in O. marina. Karlodinium
protects itself from the membrane-disrupting properties of
its own toxins by possessing a membrane sterol that does
not interact with the lipophilic compounds [16].
The possibility that the ingestion behaviour of O. marina
may be related to the bioaccumulation of noxious compounds contained within prey items is exemplified by a
recent study with the toxic raphidophyte Heterosigma
akashiwo [13]. Following experimental work with a range
of protist grazers, it was concluded that Heterosigma
toxicity was not associated with the exposure of grazers to
filtrate from the raphidophyte or with the presence of
uningested H. akashiwo in the batch-culture environment.
Instead, the toxic effect of H. akashiwo appears to depend
on ingestion of the cells [13]. Pertinently, Amphidinium
longum, a protozoan species that feeds via myzocytosis
(i.e., by piercing the cell wall of prey cells with a feeding
tube, and withdrawing their contents), is not susceptible to
A model for the chemical defence ecology of dimethylsulfoniopropionate (DMSP)-producing microalgae was first
described some 10 years ago [74]. Briefly, highly concentrated acrylate (a by-product of enzymatic degradation of
algal DMSP) is released when DMSP-producing microalgae are predated by protozoan grazers [74]. It is
postulated that acrylate deters grazing through its antimicrobial activity [60]. However, the possibility that other
noxious compounds may be implicated in the defence
reaction has been acknowledged; the toxic reactive oxygen
species superoxide (O2− [22]) is one such compound.
Superoxide production has recently been reported in a
number of marine microalgae, including toxic and DMSPproducing species (e.g., I. galbana [35]); however, the
implication/s of its production have received little attention.
Superoxide anions are released by phagocytic cells during
phagocytosis [4, 20, 45], and O2− radicals are known to
reduce the growth of bacteria [8, 17], causing conformational changes (and loss of activity) in proteins [62].
Pertinently, superoxide release by the marine microalgae
Chattonella marina and H. akashiwo is exacerbated
following stimulation of cells with a plant lectin derived
from the jack bean Canavalia ensiformis (Con A [47]); this
lectin is specific for cell-surface mannose residues. It has
been proposed that Con A may induce membrane perturbation by redistributing receptor molecules on the surface
of algal cells, resulting in activation of redox enzymes that
are required for the generation of superoxide [47]. Given
evidence to suggest that (lectin-like) mannose-specific
feeding receptors are implicated in the process of prey-cell
adhesion and biorecognition by O. marina [78], it is
entirely possible that lectin-stimulated O2− production
could constitute a novel model for grazing-activated
Figure 5 Conceptual bases for grazing-activated release of chemicals
(e.g., superoxide anions [O2–]) from A nitrogen-sufficient and B
nitrogen-limited microalgae. Binding of predator-surface feeding
receptors [78] and/or dissolved labelling molecules [54] to preysurface glycoconjugates could trigger higher levels of O2− release from
certain microalgae [35, 37, 47]
Grazing-Activated Chemical Defence: A New Model
Prey Biorecognition and Feeding in Oxyrrhis marina
chemical defence (Fig. 5). It follows that when the lectinlike feeding receptors of phagotrophic protozoa bind to
prey-surface carbohydrates, superoxide may be released
from prey cells in an oxidative burst which deters
phagotrophic ingestion. Enhanced levels of O2− production
may be associated with poor quality prey items (e.g.,
nitrogen-limited I. galbana) because they are richer in the
cell-surface (mannose-linked) glycoconjugates that lectinlike feeding receptors on phagocytic cells interact with [37,
78] (Fig. 5b).
Afterword and Future Work
This article has focused on conceptual bases for the
biorecognition of individual prey items by the planktonic
marine phagotroph O. marina. Considering the parallels
between phagocytosis in metazoan and protozoan cells, the
prospect of elucidating self and nonself recognition mechanisms in the latter remains an exciting avenue for future
research. Because it is easily accessible and readily
culturable, O. marina remains an ideal organism with
which to study molecular-level controls on phagotrophy.
However, given the diversity of marine protozoa (including
benthic, motile and nonmotile species) and their trophic
strategies (heterotrophy, mixotropy, osmotrophy, paliumfeeding, peduncle-feeding, etc.), it is clear that there
remains much to discover about the factors which influence
the outcome of microbial predator–prey interactions. A
multidisciplinary approach (including immunological, proteomic and genetic techniques) towards a wider number of
protozoan and prey species is now required.
Acknowledgements The author wishes to acknowledge the funding
of the Natural Environmental Research Council (NERC, UK) and
advice from Kevin Flynn.
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