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HORIZONS
Mechanisms underlying chemical
interactions between predatory
planktonic protists and their prey
EMILY C. ROBERTS 1*, CATHERINE LEGRAND 2, MICHAEL STEINKE 3 AND EMMA C. WOOTTON 1
1
2
DEPARTMENT OF BIOSCIENCES, SWANSEA UNIVERSITY, SINGLETON PARK, SWANSEA SA2 8PP, UK, SCHOOL OF NATURAL SCIENCES, LINNÆUS UNIVERSITY,
3
S-39182 KALMAR, SWEDEN AND DEPARTMENT OF BIOLOGICAL SCIENCES, UNIVERSITY OF ESSEX, WIVENHOE PARK, COLCHESTER CO4 3SQ , UK
*CORRESPONDING AUTHOR: [email protected]
Received July 31, 2009; accepted in principle January 12, 2011; accepted for publication January 17, 2011
Corresponding editor: John Dolan
Predatory protists use chemical recognition to increase feeding efficiency by
responding to point sources of prey chemoattractants and through adhering to the
cell surface of their prey. In response, their prey possess a multitude of chemicalbased antipredator strategies. Given that these chemical interactions play a key role
in driving aquatic food webs, we emphasize the need for a better knowledge of the
associated underlying mechanisms. As the mechanisms underpinning such chemical interactions have been intensively researched for certain non-planktonic model
protists, we highlight that studies on these model organisms can help elucidate the
mechanisms involved in planktonic predator– prey interactions. A related future
challenge will be to interpret the evolutionary and ecological consequences of these
chemical interactions within planktonic communities, and here this will be discussed in relation to coevolutionary arms races and costs.
KEYWORDS: feeding; defence; arms race; receptors; coevolution; protists; plankton; chemical; ciliates; flagellates
I N T RO D U C T I O N
There is now a wealth of research implicating chemical
involvement in the interactions that occur between protist
predators and their prey (Cembella, 2003; Pohnert et al.,
2007; Montagnes et al., 2008). From a predator perspective, these chemical interactions include responses to
point sources of dissolved chemical cues released from
prey in addition to cell surface recognition of prey
(Montagnes et al., 2008). Chemical interactions between
phagocytic protists and their prey, however, are far from
unidirectional as prey species have developed numerous
chemical antipredator strategies that aid survival (Wolfe,
1998; Strom, 2008). Surprisingly, little is known about the
potential mechanisms involved in these chemical interactions and as a consequence we lack fundamental information regarding how aquatic food webs operate.
In this Horizons article, we briefly examine the types
of chemical interaction that occur between planktonic
protist predators and their prey. It is not our intention
to provide a detailed review of these interactions, as our
main aim is to emphasize the potential underlying
mechanisms involved. In recent years, advances have
doi:10.1093/plankt/fbr005, available online at www.plankt.oxfordjournals.org. Advance Access publication February 19, 2011
# The Author 2011. Published by Oxford University Press. All rights reserved. For permissions, please email: [email protected]
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been made in identifying the receptors and cell signalling pathways driving key cellular processes for certain
model protists, including the soil-dwelling social
amoeba Dictyostelium discoideum and the enteric parasitic
amoeba Entamoeba histolytica (Shpakov and Pertseva,
2008). We propose that studies on these model eukaryotic cells can be used to shed light on the potential
mechanisms involved in aquatic microbial predator–
prey interactions. We also consider whether theoretical
approaches developed to investigate terrestrial plant –
herbivore interactions provide a useful framework for
determining the ecological and evolutionary consequences of these chemical interactions within planktonic
communities.
Chemical detection of prey by protist
predators
Cell-surface recognition of prey by phagocytic protists
Although planktonic protists can discriminate between
similar-sized prey based on differences in cell surface
composition (Montagnes et al., 2008 and references
therein), the molecular mechanisms behind this discrimination are poorly understood. Thus, it is useful
to consider alternative model systems for which cell –
cell interactions have been intensively studied. For
example, it is known from non-planktonic eukaryotic
model cells that phagocytosis is initiated by receptors
on the surface of the phagocytic cell adhering to the
prey/particle to be ingested (Bozzaro et al., 2008;
Cosson and Soldati, 2008). These receptors often
belong to common protein groups, including integrins
(heterodimeric adhesion receptors, Hynes, 2002;
Dupuy and Caron, 2008) and lectins (carbohydratebinding proteins that agglutinate cells, Lis and
Sharon, 1998). While integrins bind to a wide variety
of different ligands (Hynes, 2002), lectins can be
highly specific in their carbohydrate-binding affinity
(Lis and Sharon, 1998), thus providing different roles
in microbial recognition.
Although integrins and their associated proteins were
thought to be specific to metazoans, they are now known
to be present in some protists (Sebé-Pedrós et al., 2010).
In the terrestrial social amoeba, Dictyostelium discoideum,
SibA (similar to integrin b) appears to be the main membrane receptor responsible for adhesion to bacteria
(Cornillon et al., 2006). SibA possesses structural and
functional similarities to metazoan integrin b chains,
and the involvement of SibA in bacterial adhesion and
phagocytosis in D. discoideum appears remarkably similar
to integrin-dependent phagocytosis in mammals
(Cornillon et al., 2006; Cosson and Soldati, 2008). These
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studies are relevant to planktonic predator–prey interactions as they identify integrins and closely related proteins as candidate receptors for prey adhesion (Fig. 1). It
is tempting to question the extent to which methodological approaches developed for D. discoideum can be
adapted for use on environmentally relevant planktonic
species. One of the main advantages of D. discoideum is its
fully sequenced genome, making this model species a
powerful system for analysis (see http://dictybase.org for
standard protocols). Optimistically, though, genome
sequencing has recently been prioritized for aquatic protists (Caron et al., 2009). As a consequence, providing
differences in motility and adhesion can be overcome,
the rapidly advancing technology used to investigate
phagocytosis and bacterial adhesion in D. discoideum may
soon become relevant for planktonic protists.
A second group of proteins that function as key
adhesion and phagocytic receptors are lectins (Lis and
Sharon, 1998). A classic metazoan example is the
macrophage mannose receptor. This transmembrane
lectin on phagocytic blood cells plays a fundamental
role in “non-self ” recognition by binding to glycoconjugates on the surface of invading microorganisms, mediating phagocytosis (Stahl and Ezekowitz, 1998). Protists
also exhibit lectin-dependent cell adhesion. For
example, the free-living amoeba, Hartmannella vermiformis,
uses
a
galactose/N-actetyl-galactosamine
(Gal/
GalNAc)-binding lectin to attach and uptake the pathogenic bacterium Legionella pneumophilia (Venkataraman
et al., 1997). Through using comparative techniques,
including agglutination assays and feeding inhibition
experiments, we are beginning to discover lectin receptors in planktonic protists (Fig. 1; Roberts et al., 2010).
In particular, the marine dinoflagellate Oxyrrhis marina
uses a Ca2þ-dependent mannose-binding lectin to
capture flagellate prey (Wootton et al., 2007). This, once
again, highlights that methods developed for nonplanktonic model cells provide a useful framework to
study planktonic interactions.
Predator motile response to prey dissolved
chemical cues
Protists respond rapidly to point sources of dissolved
low molecular weight organic matter in aquatic
environments, and are capable of congregating at
them within a few minutes from distances of up to
several centimetres (Fenchel and Blackburn, 1999).
The motile response of planktonic protists to prey
exudates as well as to low molecular weight molecules have been relatively well studied (e.g. Fenchel
and Blackburn, 1999; Hausmann et al., 2003, and
references therein). Chemoattractants released by the
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Fig. 1. Mechanisms underlying the chemical interactions that occur between protist predators and their prey.
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prey that benefit the receiver (the predator) and disadvantage the originator (the prey) are referred to as
kairomones (Dicke and Sabelis, 1988). Although
elegant techniques have been developed to track
swimming behaviour in response to kairomones (e.g.
Menden-Deuer and Grünbaum, 2006; Seymour et al.,
2010), little is known about the molecular mechanisms underpinning these motile responses by protist
predators. Again, insight may be gained through
investigating alternative model systems in which these
mechanisms are better understood.
Soil dwelling Dictyostelium discoideum has been used
extensively to investigate chemotaxis, as it dynamically
senses and responds to shallow external chemoattractant
gradients (Bagorda and Parent, 2008). The two main
dissolved cues that promote chemotaxis are (1) folic
acid, a bacterial by-product, and (2) cyclic adenosine
monophosphate (cAMP), a potent chemoattractant
released by other D. discoideum cells (Bagorda and
Parent, 2008). Receptors for both these chemoattractants belong to the G-protein-coupled receptor family
and mediate the majority of their effects through
heterotrimeric guanine nucleotide-binding proteins
(G-proteins) (Bagorda and Parent, 2008).
Using simple comparative approaches, similar mechanisms are beginning to be identified in planktonic organisms (Fig. 1). Hartz et al. (Hartz et al., 2008), for example,
used inhibitors to examine the involvement of signal transduction pathways in the motile response and ingestion by
the marine ciliate, Uronema sp., and the marine dinoflagellate, O. marina. In both species, protein kinase inhibitors
decreased the motile response and ingestion, while
G-protein inhibitors decreased the motile response (Hartz
et al., 2008). Their results suggest that G-protein and
protein kinase signalling pathways are involved in the
feeding behaviour of planktonic protists (Hartz et al.,
2008), providing further evidence that signalling pathways
associated with chemotaxis appear to be conserved
throughout eukaryotes (Shpakov and Pertseva, 2008).
Chemical avoidance by prey
Prey are under strong selective pressure to develop traits
needed to survive grazing and consequently, plankton
display a multitude of antipredator strategies. While
certain prey adaptations provide mechanical protection
from grazing, e.g. spines and tough cell walls (Hamm
et al., 2003; Pondaven et al., 2007), others involve chemical interactions (Fig. 1).
Cell surface antipredator properties of prey
The cell surface composition of the prey can affect
grazing susceptibility (Verity, 1988, 1991; Jürgens and
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Matz, 2002; Jezbera et al., 2005; Yang et al., 2008). For
example, Zwirglmaier et al. (Zwirglmaier et al., 2009)
investigated selective feeding of marine heterotrophic
flagellates on different strains of Synechococcus with
varying cell surface properties. The predatory flagellates
showed similar strain-specific grazing preferences,
despite using different mechanisms to acquire prey, indicating selectivity was driven by prey properties, not
feeding strategy. Further investigation revealed modification in the cell surface lipopolysaccharide layer
between grazed and grazer-resistant Synechococcus strains.
This study supports previous suggestions that cell envelope modifying genes alter cell surface characteristics of
Synechococcus, thus affecting resistance to protist predation
(Fig. 1; Palenik et al., 2006; Strom, 2008; Zwirglmaier
et al., 2009). Given the availability of Synechococcus
genomes, this genus provides a powerful model system
to further investigate candidate genes responsible for
cell surface antipredatory properties.
Use of dissolved molecules in prey protection: grazing
resistant forms
Numerous predator-avoidance tactics involve dissolved
chemicals (Fig. 1; Wolfe, 1998; Pohnert et al., 2007). For
example, dissolved substances released by protist predators can be detected by the prey, stimulating the growth
of grazing-resistant morphologies (Fig. 1). The freshwater
bacterial species, Flectobacillus sp., for instance, develops
grazing resistant forms in the presence of excretory products released by the bacterivorous flagellate, Ochromonas
sp. (Corno and Jürgens, 2006). The molecular mechanisms that trigger the growth of grazing resistant prey
morphologies are not currently known, although it is
highly likely that receptors are involved.
Use of dissolved molecules in prey protection: chemorepellents
Allomones are chemorepellents that benefit the originator ( prey) and disadvantage the receiver ( predator)
(Dicke and Sabelis, 1988). Some ciliates possess
allomone-containing extrusive organelles that discharge
upon contact with predators (Harumoto et al., 1998;
Miyake et al., 2001, 2003). The freshwater heterotrich,
Climacostomum virens, for example, discharges toxins from
cortical granules in response to proboscis contact of the
raptorial ciliate, Dileptus margaritifer, resulting in rapid
retreat of the predator (Miyake et al., 2003).
Again, receptor– ligand interactions have been shown
to trigger the motile response of predatory protists away
from chemorepellents (Fig. 1; Robinette et al., 2008). In
the freshwater ciliates, P. tetraurelia and T. thermophila,
polycation receptors are involved in the detection of
numerous chemorepellents (Robinette et al., 2008).
Polycation reception in P. tetraurelia appears to be
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mediated through a tyrosine kinase pathway (Robinette
et al., 2008). In contrast, the polycation receptor in
T. thermophila signals through a G-protein coupled
pathway (Hassenzahl et al., 2001; Keedy et al., 2003). In
the presence of chemorepellents, both P. tetraurelia and
T. thermophila exhibit a distinct avoidance response,
characterized by reorientation of their swimming direction and jerky backward swimming (Robinette et al.,
2008). Through knowing the underlying molecular
mechanisms involved in the response to chemorepellents, the observed behaviour of the protist predators
can be better understood.
Certain dinoflagellates and haptophytes produce lytic
compounds that inhibit feeding of heterotrophic protists
(e.g. Tillmann, 2003; Adolf et al., 2007; Tillmann et al.,
2009). For example, karlotoxins produced by the marine
mixotrophic dinoflagellate, Karlodinium veneficum, induce
the formation of pores within the cell membrane of
protist predators (Fig. 1; Deeds and Place, 2006; Adolf
et al., 2007). The susceptibility of protist grazers to karlotoxin can be predicted based on their membrane sterol
composition (Deeds and Place, 2006). Knowing the
mode of action of antipredatory compounds, therefore,
provides tools for further research on the understanding
of harmful algal bloom dynamics.
Use of dissolved molecules in prey protection: multitrophic
interactions
The role of dimethylsulphoniopropionate (DMSP) in
planktonic trophic interactions is topical; here we highlight its potential for affecting multitrophic interactions,
although undoubtedly other examples exist in planktonic systems. Although bulk additions of DMSP inhibit
grazing by certain protist grazers (Strom et al., 2003),
gradients of DMSP appear to attract them (Breckels
et al., 2010b; Seymour et al., 2010). DMSP can be enzymatically cleaved to produce the trace gas dimethyl sulphide (DMS) and this has been suggested to act as a
chemoattractant that may benefit prey communities
indirectly (Steinke et al., 2002). Plumes of DMS are produced when protist predators feed on certain marine
phytoplankton species including coccolithophores
(Wolfe et al., 1997). A study investigating the tail-flapping
response in the marine copepod Temora longicornis has
led to the suggestion that DMS acts as an infochemical,
used by mesozooplankton to detect and locate potential
protist prey (Steinke et al., 2006). It has been proposed
that mesozooplankton can utilize the directional information provided by grazing-activated DMS to locate
their prey. As a result, protist herbivores will be more
susceptible to predation and this will enhance the
ability of DMS-producing phytoplankton to establish
dense populations (Pohnert et al., 2007). Intriguingly,
many successful and bloom-forming phytoplankton taxa
are strong producers of DMSP and DMS, including
many dinoflagellates, and the marine haptophytes
Phaeocystis sp. and Emiliania huxleyi. Although the mechanisms involved in the detection of DMS and DMSP by
planktonic organisms are not currently known, studies
on model protists provide candidate receptors worthy of
further investigation (see “Predator motile response to
prey dissolved chemical cues” above).
Chemical interactions, planktonic
communities and coevolution
Determining the ecological and evolutionary consequences of predator–prey chemical interactions in planktonic communities is clearly the next big challenge. To
demonstrate different chemical interactions we have
mainly considered predator–prey pairs. When presented
in this context, one might question the extent to which
these interactions act as a chemical arms race (Dawkins
and Krebs, 1979; Smetacek, 2001), with participants consistently developing adaptations and counter-adaptations.
In terrestrial systems, such chemical arms races occur
among tightly coupled predator–prey pairs (e.g. wild
parsnip and parsnip webworm, Berenbaum and Zangerl,
1998, and garter snakes and newts, Brodie and
Ridenhour, 2002; Geffeney et al., 2002). These specialized
couplings result in pairwise coevolution that can lead to
the rapid evolution of extreme traits, high degrees of
specialization and new species (Brodie and Ridenhour,
2002; Geffeney et al., 2002). We argue that within planktonic communities, examples of pairwise coevolutionary
arms races are probably rare. They are most likely to exist
among taxa exhibiting highly selective feeding strategies,
such as marine mixotrophic dinoflagellates and their prey
(e.g. Fragilidium subglobosum, Skovgaard, 1996; Hansen and
Nielsen, 1997). In such relationships, a coevolutionary
arms race can only occur if the predator exerts substantial
grazing pressure on prey populations (e.g. Jeong et al.,
2005). Within planktonic communities, pairwise coevolution is more likely to arise between highly specific protist
parasites and their hosts (e.g. marine parasites Pirsonia
spp. and Amoebophrya spp., Tillmann et al., 1999;
Chambouvet et al., 2008). If the molecular mechanisms
underlying these host-parasite and predator–prey interactions can be identified, coevolutionary changes in the
proteins involved can be detected using statistical
approaches (e.g. Fares and Travers, 2006), providing a
mechanism to test their prevalence.
The majority of planktonic predator–prey chemical
interactions are, undoubtedly, more general than those
described above. Although planktonic protist predators
are capable of prey selectivity, they often graze on
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multiple species, and their prey recognition is likely to
reflect this (Montagnes et al., 2008). Equally, secondary
metabolites released by phytoplankton that deter protist
grazing also frequently serve an allelopathic role, killing
phytoplankton competitors (Legrand et al., 2001;
Tillmann, 2004; Tillmann et al., 2008). Within these generalized, multispecies interactions, if coevolution occurs,
it will be diffuse rather than pairwise (Janzen, 1980;
Strauss and Irwin, 2004). For terrestrial plant–herbivore
interactions, theoretical models and experimental designs
for distinguishing between pairwise and diffuse selection
and coevolution have been well developed (Strauss et al.,
2005). We suggest that it may prove useful to apply
similar criteria to planktonic predator–prey interactions.
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Costs to prey
For prey, there is currently debate regarding the energetic
cost of predator avoidance tactics. Producing secondary
metabolites for defence and allelopathy has generally
been considered energetically costly (e.g. Strauss et al.,
2002; Pohnert et al., 2007; Flynn, 2008). However, this
may not always be the case (Tillmann et al., 2009).
Among different clones of the marine dinoflagellate
Alexandrium tamarense, no correlation was found between
allelochemical potency and growth rate (Tillmann et al.,
2009). This indicates that, under non-limiting growth
conditions, no obvious growth costs are associated with
the production of lytic secondary metabolites in this
species. Given that direct and ecological costs of defence
can be complex and difficult to detect (Strauss et al.,
2002), this is clearly an avenue for continued research.
Counting the costs
To interpret the ecological and evolutionary relevance
of protist predator– prey chemical interactions, it is
essential to consider their costs. Again, theoretical and
methodological approaches developed to investigate
costs of resistance within terrestrial plant – herbivore
interactions provide a useful framework (Strauss et al.,
2002). In terms of direct allocation or resource-based
costs, it may not always be advantageous to invest in
producing sophisticated prey recognition apparatus and
antipredator chemicals. Also there are indirect, or ecological, costs that require interactions with other species
to be expressed. These costs include increased impact of
enemies (e.g. viruses, parasites), reduced tolerance to
enemies and reduced intra- or interspecific competitive
ability (Strauss et al., 2002).
Costs to predators
For predatory protists, direct costs associated with prey
recognition will vary depending on the feeding strategy
used. Predatory protists employ an array of feeding
strategies, enabling ingestion of different prey types and
sizes (Boenigk and Arndt, 2002; Hausmann, 2002;
Tillmann, 2004). Many dinoflagellates are specialized
predators (Hansen and Calado, 1999; Tillmann, 2004;
Sherr and Sherr, 2007); therefore, relatively high energy
investment in prey recognition would be expected. In
contrast, bacterivorous filter feeding ciliates are much
less selective and are frequently referred to as indiscriminate feeders (e.g. Fenchel, 1980). Although a lower
energy investment in prey recognition might be
expected for these filter feeders, there is mounting evidence that chemosensory and behavioural mechanisms
are employed to discriminate between different food
particles (Sanders, 1988; Christaki et al., 1998; Wilks
and Sleigh, 1998; Thurman et al., 2010).
CONCLUSION
Chemical interactions with their prey enable protistan
predators to increase feeding efficiency, both through a
motile response to prey exudates and by cell surface recognition. The extent to which different protist species
rely on these chemical interactions varies, and through
employing a multitude of diverse feeding strategies,
these highly efficient predators are able to occupy many
different feeding niches. As a consequence, prey are
under strong selective pressure to develop chemical and
physical traits needed to survive grazing. Gaining a
better understanding of the molecular mechanisms
underpinning these chemical interactions is of critical
importance given the widely accepted view that planktonic protist grazers play a fundamental role in the
functioning of aquatic food webs.
In this Horizons article, we emphasize that receptor–
ligand interactions play a vital role in driving chemical
interactions within aquatic microbial food webs. Given
that mounting evidence indicates that many aspects of
the mechanisms involved in phagocytosis and chemotaxis are conserved across the eukaryotic tree of life
(Bagorda and Parent, 2008; Bozzaro et al., 2008;
Shpakov and Pertseva, 2008), we can learn much from
studies on non-planktonic model protists, particularly in
respect to identifying candidate molecules that warrant
further investigation. Currently, the application of basic
techniques to identify receptors and signalling pathways
involved in feeding by planktonic protists has provided
support to this theory (e.g. Wootton et al., 2007; Hartz
et al., 2008). As the availability of sequenced genomes
multiplies, powerful molecular approaches originally
developed for non-planktonic model cells will become
increasingly applicable to planktonic protists.
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Determining the broader ecological and evolutionary
consequences of these planktonic predator–prey chemical
interactions remains complicated. Although the theoretical
and methodological approaches developed for terrestrial
plant–herbivore interactions may provide a useful framework, the evolutionary and ecological outcome of these
predator–prey chemical interactions are likely to differ
considerably between aquatic and terrestrial environments. Differences in physical and chemical characteristics
between terrestrial and aquatic environments have considerable consequences in relation to how chemical cues
are conveyed. Furthermore, marine, freshwater and terrestrial ecosystems inherently differ in terms of their scales,
connectivity and degree of organism specialization within
them, which has important implications for food web
complexity (Link, 2002). Given the complexity of planktonic food webs, the high diversity of nutritional modes
used by planktonic organisms and the ability of planktonic
protists to feed on multiple prey species, untangling and
interpreting the evolutionary and ecological relevance of
this intricate predator–prey chemical web is likely to prove
highly challenging, but ultimately rewarding.
AC K N OW L E D G E M E N T S
The Authors would like to thank Thomas Kiørboe for
his encouragement and invitation to write this Horizons
article and Kristina Hamilton for her constructive comments. We also thank David Montagnes and two anonymous reviewers for their helpful suggestions and Roger
Harris and Lulu Stader for their endless patience.
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FUNDING
This work was, in part, supported by: UK NERC
grants NE/C519438/1 and NE/G010374/1 awarded
to E.C.R., and NE/H009485/1 to M.S., European
Commission grants FP7-PEOPLE-220732 (ALGBAT),
and
Swedish
Research
Council
Formas
(ECOCHANGE) awarded to C.L.
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