AMER. ZOOL., 29:399-407 (1989)
Determinants of Compatibility in Mollusc-Trematode Parasitism 1
CHRISTOPHER J. BAYNE
Department of Zoology, Oregon State University,
Corvallis, Oregon 97331
AND
TIMOTHY P. YOSHINO 2
Department of Zoology, University of Oklahoma,
Norman, Oklahoma 73019
SYNOPSIS. The low prevalence of schistosome-infected snails in hyperendemic habitats,
and the demonstrated ability of snails, in general, to recognize and eliminate a myriad of
foreign substances and/or infectious agents, lead to the postulate that host resistance to
larval trematodes must be considered the "rule," while susceptibility (compatibility) represents an exceptional occurrence. In this review, we discuss a variety of possible mechanisms by which compatibility between trematodes and their molluscan host might be
attained. Included among these are parasite mimicry of snail host molecules, prevention
of opsonization, interference with hemocyte behavior or differential stimulation of hemocyte metabolic processes. Evidence that compatibility is the result of the ability of larvae
to resist toxic host molecules or to acquire protective host components on their surface
membranes is lacking. Clearly, there are multiple variables of both host and parasite
origin which ultimately determine compatibility. Careful identification and dissection of
these variables will be required before we achieve a complete understanding of how
compatible snail-trematode associations are established and maintained.
INTRODUCTION
Molluscs have tremendously effective
internal defense systems. Anything entering the body of a mollusc immediately
encounters the hemocytes and plasma
which constitute the blood (hemolymph) in
these animals with open or hemocoelic circulatory systems. From early studies of the
fate of materials experimentally injected
or implanted into molluscs, it is clear that
practically all foreign materials are either
phagocytosed or encapsulated (Stauber,
1950; Tripp, 1961). More recent studies
of clearance rates of injected bacteria, yeast,
erythrocytes or proteins confirm that molluscs have a high capacity to recognize and
clear paniculate or soluble foreign substances from their hemolymph (Bayne,
1974, 1982; Crichton and Lafferty, 1975;
' From the Symposium on Phylogeny of Immune
Defense Mechanisms in Parasitic Infections presented at
the Annual Meeting of the American Society of Zoologists, 27-30 December 1987, at New Orleans, Louisiana.
* Current address: Department of Pathobiological
Sciences, University of Wisconsin-Madison, 2015
Linden Drive West, Madison, Wisconsin 53706.
Renwrantz et al., 1981; van der Knaap et
al., 1981).
Even when we examine the fates of larval trematodes, we find that, in many cases,
miracidia which penetrate a mollusc fail to
establish infections. In natural ecosystems,
individual snails frequently harbor a relatively small proportion of the trematode
species whose infective larvae share the
same body of water. In fact, in order for a
trematode to establish a successful infection in a mollusc, special conditions must
prevail.
The inescapable conclusion is that resistance to foreign agents is the rule; compatibility of host and parasite is the exception. This becomes intuitively obvious when
we consider that wild populations of molluscs (and practically all other organisms
as well) live in the midst of numerous
potentially infective foreign agents, yet are
healthy. From an evolutionary perspective,
selection would be expected to favor host
phenotypes "resistant" to particular parasites, especially those which negatively
impact host populations by causing high
morbidity or mortality.
As we consider compatibility in mollusc—
399
400
C. J. BAYNE AND T. P. YOSHINO
TABLE 1. Phenomena which may explain compatibility inparasite and
molluscan schistosomiasis.
which has led
host into "concordance,"
us to ask the question, "What
determines compatibility?"
1. Sporocysts resist toxic components of the host.
Perhaps the question, "What determines
2. Sporocysts avoid being recognized due to:
compatibility?" is really better phrased
a. Molecular mimicry
b. Acquisition of host molecules
"Which factors in both trematode and
c. Prevention of opsonization
mollusc must be concordant?" To know
3. Sporocysts interfere with host hemocyte function.
how best to approach this question, we need
to know what happens when trematodes
penetrate molluscs with which they are not
trematode parasitism, it is important to concordant. In brief, miracidia transform
realize that incompatibility in the form of into primary sporocysts which are quickly
resistance or unsuitability is nonspecific, encapsulated and destroyed by hemocytes
and that compatibility {i.e., susceptibility to (see review by Bayne, 1983). The ability of
infection) is specific. Compatibility requires the host hemocyte to recognize and kill
that the host is capable of satisfying the invading larvae is of central importance in
physiological needs of the parasite, and mediating anti-parasite responses. Howlacks resistance. It also requires that the ever, what is not as clear is whether incomparasite is infective for the compatible host. patibility or nonconcordance is based only
Both resistance and infectivity are under on the presence of host resistance factors,
genetic control (see reviews by Loker and or the absence of larval infectivity factors,
Bayne, 1986; Lie et al., 1987). Observing or a complex combination of both.
that the fates of miracidia entering snails
In Table 1 we present a framework for
were predictable, even when two miracidia consideration of the various mechanisms
of different infectivities simultaneously which might operate to assure compatibilpenetrated an individual snail, Basch (1975) ity in mollusc-trematode parasitism. In our
postulated that "a concordance, e.g., of discussion of the outlined topics, it should
genetically determined antigen groupings be kept in mind that most of the available
between host and successful parasite," must information has resulted from studies utiexist for compatibility to be manifest. While lizing a limited number of parasite-host
we might now prefer to talk of "charac- models, primarily the schistosomes or echiters" instead of "antigen groupings," nostomes and their freshwater gastropod
research since 1975 (e.g., Kassim and Rich- hosts. Therefore, one must be cautious in
ards, 1979) has tended to support Basch's extrapolating the reported findings and
notion.
interpretations to all trematode-mollusc
The late Dr. C. A. Wright performed an systems. Because of this relatively narrow
experiment (Wright, 1974), later substan- focus on a few systems, we feel there is a
tiated by Rollinson and Southgate (1985), strong need to expand investigations into
which tells us important things about the other less "traditional" models to begin
basis of compatibility in mollusc-trema- broadening our view of how snails and their
tode systems. He found a population of trematodes achieve compatibility.
Schistosoma matheei which developed in BuliRESISTANCE TO TOXIC COMPONENTS
nus globosus, but not in B. scalaris. The
related schistosome, S. intercalatum, develEvidence fails to support the possibility
oped in B. scalaris, but not in B. globosus. that sporocysts resist toxic components of
When Wright crossed the two schistosome the host. Light and electron microscopical
species, the F, offspring were infective for studies have shown repeatedly that spoboth species of Bulinus. Apparently, a rocysts in compatible infections do not elicit
recombination of genes now expressed in a host attack. In general, encapsulation—
hybrid offspring compensated for the the landmark of incompatible infections—
parental inability to infect reciprocally does not occur. If structural studies had
these snail hosts. It is the intriguing nature revealed that sporocysts were surviving in
of this genetic "compensation," bringing the face of cellular encapsulation, we might
MOLLUSC-TREMATODE COMPATIBILITY
401
conclude that they were resistant to the cysts, which we have found to occur in
attack. As to toxic components of host plasma, could be due to the simultaneous
plasma, there appear to be none potent binding of plasma components by neighenough to seriously damage sporocysts. We boring sporocysts. For this reason we found
have observed that Schistosoma mansoni pri- it necessary to fix sporocysts before submary sporocysts do well in plasmas from jecting them to agglutination tests (Loker
either susceptible or resistant strains of et al., 1984). When 5. mansoni sporocysts
Biomphalaria glabrata (Bayne et al., 1980a, were fixed, blocked and placed in B. glab). Thus, compatibility does not appear to brata plasma, they agglutinated in the
be based on the ability of sporocysts to resist plasma from resistant strains of snail, and
toxic host molecules.
not in that from susceptible strains. We
were unable to inhibit sporocyst agglutiAVOIDANCE OF RECOGNITION
nation with carbohydrates, so remain silent
on
the question of the possible lectin nature
The fact that sporocysts in compatible
of
the
agglutinin. However, the fact that
infections fail to elicit encapsulation
responses supports the notion that the par- resistant strain plasmas in this host-parasite
asites avoid being recognized by the inter- model also possess the ability to bestow a
nal defense system of the host. In order to cytotoxic capacity in normally benign, susevaluate this possibility, a review of what ceptible snail hemocytes in vitro (Bayne et
we know of the non-self recognition sys- al, 19806) and can transfer resistance in
tems operating in molluscs is now pre- vivo (Granath and Yoshino, 1984) clearly
implies a potential "immune-type" recogsented.
nition function for this or other plasma
factors. Precedent for such a role exists in
Recognition systems in molluscs
In the absence of immunoglobulins, mol- the mononuclear phagocyte system of Helix.
luscan recognition factors are likely to be Renwrantz et al. (1981) found that the
lectins (reviewed by Renwrantz, 1986). clearance of yeast injected into this land
Lectins with more than one carbohydrate- snail was slowed by the simultaneous injecbinding site will agglutinate particles bear- tion of n-acetyl-d-glucosamine or n-acetyling those determinants on their surfaces. d-galactosamine, which appear to be blockIt has long been known that molluscan body ing receptors on the snail's phagocytes.
fluids are rich sources of agglutinins for Furthermore, hemocytes of the mussel,
vertebrate erythrocytes {e.g., Pauley, 1974; Mytilus edulis, and the oyster, Crassotrea virStanislawskitf/a/., 1976). Like invertebrate ginica, express lectins on their surface
hemagglutinins in general, these sub- membranes which are capable of binding
stances are inhibitable by specific carbo- to or agglutinating various foreign partihydrates. Foreign organisms which are cles including yeast or vertebrate erythlikely to be encountered by molluscan rocytes (Renwrantz and Stahmer, 1983;
hemocytes are certain to express surface Vasta et al, 1984). The recent report (Fryer
carbohydrates, so a lectin-based recogni- et al, 1989) that mannan blocks opsonition system should be useful. Indeed, we zation and laminarin blocks phagocytosis
have direct evidence of the existence of in a B. glabrata-yeast model further bolsugars on the surfaces of trematode pri- sters the notion that lectins are widespread
mary sporocysts, the larval stage at which "immune-type" recognition factors in molcompatibility is first established in molluscs luscs.
(Yoshino et al, 1977; Boswell et al, 1987;
van der Knaap et al, personal communi- Molecular mimicry
cation).
With this background, let us return to
Do lectin-type agglutinins recognize the postulate that compatibility in moltrematodes in molluscs? The tegument of lusc-trematode systems is assured by
a sporocyst is its nutritive surface, respon- avoidance of recognition. After thorough
sible for the uptake of nutrients from host analysis of the available data, Yoshino and
plasma; therefore clumping of live sporo- Boswell (1986) concluded that "In trema-
402
C. J. BAYNE AND T. P. YOSHINO
INFECTIONS OF Oncomelania SNAILS
IMMUNOPRECIPITINS:
BY S. iaponicum. CHINESE STRAIN
SNAIL SUBSPECIES
Anti-S. iaponicum adults
INFECTION RATE* (%>
O. hupensis hupensis
59-60
O. hupensis nosophora
45-49
O. hupensis chiui
20-21
Q. hupensis quadrasi
0
O. hupensis formosana
0
Antigens:
Q. hupensis subspp.
I
FIG. 1. Correlation between laboratory infection rates of various Oncomelania hupensis subspecies and the
number of snail antigens for each subspecies which crossreact with an anti-Schistosoma japonicum adult worm
antiserum. The Chinese strain of 5. japonicum was used in snail infection trials and in generating the adult
worm antiserum. Note that, in general, high, moderate and low rates of snail infection correspond to high
(many), moderate and low (few) numbers of antigens (immunoelectrophoretic arcs) shared between parasite
and snail host. (Compiled from Fig. 1 and Table 1; Iwanaga and Tsuji, 1985)
tode—mollusc systems there is no evidence
for a parasite protective role of mimicked
molecules." But how strongly does the evidence implicate mimicry? Figure 1 shows
the correlation which was found when
Iwanaga and Tsuji (1985) quantified both
infectivity and shared antigens in the Schistosoma japonicum-Oncomelania
hupensis sys-
tem. The fact that high, intermediate and
low levels of compatibility correlate with
high, intermediate and low numbers of
shared antigens calls for us to keep open
minds on the question of a protective role
for shared antigens, although direct evidence is still lacking. A similar observation
of higher immuno-crossreactivity between
a compatible host and parasite when compared to a resistant host-parasite combination was made earlier in an S. mansoniBiomphalaria system (Yoshino and Bayne,
1983).
Of course, vertebrate antibodies do not
reveal antigens so much as they reveal epitopes. Hence, immuno-crossreactivity must
be interpreted as demonstrating shared
epitopes (not antigens), at least until such
cross-reactive moieties are further characterized by methods such as Western blotting (Bayne et ai, 1987). Despite this reservation, it remains important to answer such
questions as "Might one or more of the
shared epitopes seen uniquely in the most
susceptible 0. hupensis-S. japonicum system
be involved in compatibility?"
Acquisition of host molecules
Since Yoshino and Boswell's analysis
(1986), few new data are available concerning the potential role of acquired host
molecules in mediating larval avoidance of
immune detection. Our studies of antigen
acquisition by primary sporocysts in snail
plasma (Bayne et al., 1986; Yoshino and
Boswell, 1986), using antibodies as probes,
revealed extensive binding of plasma components under in vitro conditions. More
recently, Bayne and Hull (1988) probed
sporocyst surfaces with NHS-Biotin, which
labels peptides, and found little change
when sporocysts encountered plasma. This
remains enigmatic. Regardless, the conclusion that acquired antigens play no functional role in larval trematode protection
is strongly substantiated by observations
made using in vitro cytotoxicity assays
(Loker and Bayne, 1982): 5. mansoni sporocysts preincubated in cell-free plasma
from susceptible strain B. glabrata, then
placed in culture with hemocytes from a
resistant B. glabrata strain, all in the presence of susceptible snail plasma, were killed.
Clearly, susceptible strain plasma did not
protect sporocysts from the cytotoxic
capacity of the hemocytes. Similarly, injec-
MOLLUSC-TREMATODE COMPATIBILITY
tion of susceptible B. glabrata plasma into
resistant snails or preincubation of primary
sporocysts in susceptible plasma prior to
injection of these parasites into resistant
hosts failed to protect parasites upon entry
into the snail (Granath and Yoshino, 1984).
It is fair to conclude that acquired host
molecules do not protect trematodes within
their molluscan hosts, at least as evidenced
by in vitro studies.
403
ously reported. Future studies of opsonization in molluscs need to pay attention to
the kinetics of the process.
Insights derived from these new observations have yielded a new hypothetical
mechanism for compatibility in mollusctrematode parasitism, viz., compatibility
may occur when a sporocyst avoids or
aborts the process of opsonization. The
notion is that, like yeast, sporocysts at first
acquire host plasma proteins which are initially protective (as seen by negative opsonic
Prevention of opsonization
values). The later "maturation" of opsonIf phagocytosis and encapsulation are ization requires the presence in the plasma
manifestations of the same cell behavior of a component which binds specific (car(adherence and spreading over foreign bohydrate?) components on the sporocyst.
surfaces), then we can use a phagocytosis Compatibility is the result of the absence
assay as a model of hemocyte responses to on larvae of determinants which are rectrematodes. Recently, interesting details of ognized by the opsonizing factors of that
an opsonic system in B. glabrata have been snail. Resistance that is manifested by in
revealed (Fryer and Bayne, 1989). Yeast vitro killing of sporocysts in the absence of
can be phagocytosed in saline without ever plasma components (Bayne et al., 1980a, b)
having had contact with snail plasma. How- is postulated to be due to constitutive heever, the plasma from strains of B. glabrata mocyte receptors for native determinants
which are resistant to the PR1 strain of S. on the sporocyst surface.
mansoni will opsonize yeast in a time-depenOur suggestion is that trematodes may
dent process with interesting kinetics. achieve infectivity for a particular mollusc
Hemocytes from both resistant and sus- by failing to elicit, or by blocking, the
ceptible snail strains have receptors for the opsonization process. This is consistent with
opsonized yeast, although plasma from sus- experimental data obtained using in vitro
ceptible snails lack the opsonin! A novel CMC assays in which resistant strain plasma
aspect of our findings is that exposure of bestows cytotoxic capacity on susceptible
yeast to either resistant or susceptible strain hemocytes. Our findings (Fryer and
plasma for only a few minutes reduces Bayne, 1989) that susceptible strain hemophagocytosis of these yeast. Positive opson- cytes possess receptors for the opsonin in
ization occurs only in resistant plasma, and resistant strain plasma lends further crerequires periods of about an hour. Over dence to this postulated mechanism.
this period, yeast in susceptible plasma lose
This model begs the question, "Why does
their "negative" opsonization values. a snail not produce recognition factors for
Western blot analysis of the plasma compo- all possible determinants which sporocysts
nents which are deposited on the yeast might express?" In other words, "Why does
reveals that these change over an hour, and the snail not evolve total resistance?"
although variable between experiments, Although the question is unanswered at
there are strain-specific differences in this time, we suggest that the need for a
adsorbed plasma proteins.
state of non-reactivity against self, analoThe slowed phagocytosis of yeast exposed gous to immunological tolerance, may
briefly to plasma is reminiscent of the necessitate the absence of some specificities
report that hemocyanin from Helix, if in the (lectin-based?) recognition systems
linked to the surface of yeast, slowed its of invertebrates. In this regard it is reaclearance when injected (Renwrantz et al., sonable to suggest that these "windows" in
1981). However, early negative and late the host's internal defense system may reppositive opsonic values for particles placed resent important targets for exploitation
in molluscan plasma have not been previ- by larval trematodes. Opsonic failure, for
404
C. J. BAYNE AND T. P. YOSHINO
example, may be the result of sporocyst
mimicry of dominant host carbohydrate
determinants.
TREMATODE MODULATION OF HOST
HEMOCYTE FUNCTION
Evidence that trematodes interfere with
snail hemocytes came first from the studies
of Lie and colleagues, which were masterfully reviewed by Lie in 1982, and again
by Lie et al. in 1987. Among several interesting and telling observations, Lie found
that partially resistant B. glabrata snails
harboring "escaped" infections of Echinostoma lindoense responded to a new invasion
of E. lindoense by producing large numbers
of hemocytes. Instead of accumulating
around the echinostomes, however, these
hemocytes accumulated in ectopic sites.
This appears to be not so much an analog
of vertebrate cell "migration inhibition
factor" as a forced mis-migration! This form
of interference ensures that a snail's hemocytes fail to encapsulate the parasite. Trematodes can also interfere with the cytotoxic capacity of hemocytes which do
encapsulate sporocysts. Direct evidence
supporting this notion (proposed by Lie
and colleagues) came from in vitro experiments performed by Bayne et al. (1986):
hemocytes from B. glabrata which were
infected with E. paraensei were much less
capable of killing 5. mansoni sporocysts than
were hemocytes from similar snails which
were free of echinostome infections. This
depressed immunocompetence was a manifestation of hemocyte function, not a
plasma effect. If echinostomes were present during the in vitro assay, they depressed
the cytotoxic capacity of resistant-type
hemocytes.
A possible molecular basis for trematode-mediated modulation of hemocyte
function recently has been demonstrated
by Yoshino and Lodes (1988). They have
shown that excretory-secretory (E-S)
products of cultured 5. mansoni larvae
induce an enhanced biosynthesis of hemocyte secretory polypeptides in vitro. Resistant B. glabrata hemocytes under nonstimulated and parasite-stimulated conditions
had an overall higher secretory protein
synthetic rate than comparably treated susceptible snail cells. This higher rate of synthesis, especially for polypeptides in the 50
to 180 kilodalton (kD) range, is consistent
with the notion that resistant hemocytes
are metabolically more active than those
of susceptible snails. Larval E-S products
stimulated strong increases in the secretion
of labeled 66 and 63 kD polypeptides in
hemocytes from susceptible snails. In contrast, cells of resistant B. glabrata, while
increasing the production of the 66 kD
polypeptide, experienced a decrease in the
output of the 63 kD component. The same
E-S products were without effect on the
proteins synthesized and secreted by cells
of the B. glabrata embryonic cell-line, Bge
(Hansen, 1976), suggesting that the parasite stimulatory effect may be hemocytespecific.
The schistosome E-S molecules responsible for modulating hemocyte metabolism
have yet to be identified. However, preliminary molecular fractionation and heat stability experiments indicate that several distinct larval products may be involved in
stimulating production of different groups
of hemocyte secretory proteins. For example, heat treatment (100°C for 6 min) of
parasite supernatant has no effect on its
ability to stimulate synthesis of the 66 kD
polypeptide, whereas the production of
other hemocyte proteins normally induced
by larval secretions is reduced to control
levels. This result suggests the presence of
both heat-sensitive and insensitive components comprising the E-S products of
these parasites.
Additional studies also show the possible
multiple effects of sporocyst E-S components on hemocyte activity (Lodes and
Yoshino, personal communication). When
susceptible and resistant snail hemocytes
are exposed to crude larval supernatants
in modified Boyden chemotaxis chambers,
there is a differential response in cell motility between the two snail strains. Susceptible snail hemocytes exhibit a strong
reduction in transmembrane motility in
response to larval secretions while motility
of resistant strain cells is only slightly
reduced from that of untreated controls.
However, a high molecular weight fraction
405
MOLLUSC-TREMATODE COMPATIBILITY
HOST EFFECTOR REACTIONS
CYTOTOXIC
KILLING
RECOGNITION
ACTIVAT I ON
PftRASITE ANTI-EFFECTOR
RESPONSES
PLASMA
ACTIUE
INTERFERENCE
FIG. 2. Summary of the various kinds of interaction between the snail hemocyte (principal host effector cell)
and the primary sporocyst (target stage of early host defense reactions). Solid arrows represent hemocyte or
plasma-mediated internal defense processes, while dashed arrows represent larval trematode influences on
either host effector or anti-effector activities.
of larval cuture supernatant (>30 kD),
while continuing to strongly suppress
movement of susceptible hemocytes,
appears to stimulate motility in cells of
resistant snails. A low molecular weight
fraction (<10 kD) affects the mobility of
hemocytes from both snail strains in a manner similar to the crude larval E-S preparation. These results again support the
idea that multiple molecules released from
larval schistosomes may be capable of influencing a variety of host cell activities. How
particular hemocyte populations respond
to this "mix" of E-S products probably
depends on the relative concentrations of
specific components in the test medium and
the innate sensitivity of target cell populations to these components. By isolating
specific E-S products and testing their
individual effects on hemocyte metabolism
and behavior, we hope to determine if specific larval induction (or suppression) of
selected hemocyte activities are important
in determining compatibility between
schistosomes and their snail hosts.
An emerging hypothesis evolving from
work on larval schistome E-S products is
that differences in the innate susceptibility
of snail strains to a specific trematode strain
may be a reflection of how hemocytes perceive and respond to specific molecular signals from the parasite. As suggested above,
perhaps both stimulatory and inhibitory
factors are secreted simultaneously by
invading larvae, and the "net" behavioral
response of circulating hemocytes to the
parasite may depend upon their relative
sensitivity to each factor. It might be speculated that the echinostome-induced "mismigration" of hemocytes or interference
with in vitro cytotoxic reactions are reflections of a high hemocyte sensitivity to these
suppressive influences. Thus, as summarized in Figure 2, the ultimate determi-
406
C. J. BAYNE AND T. P. YOSHINO
nation of compatibility between a given
snail and its larval trematode depends on
the shift of the balance between host effector capabilities and the sensitivity of that
system to parasite anti-effector responses.
CONCLUSIONS
It would be simplistic to think that a single mechanism operates to ensure compatibility of trematodes in molluscan hosts.
Several variables must influence the eventual outcome of each trematode-mollusc
encounter, and we postulate that compatibility is assured by a sequence of mechanisms which operate throughout the infection. We envisage that during the earliest
phase of an infection, passive mechanisms
operate, like failure to elicit opsonization.
As parasite larvae become established, they
achieve an ability to intefere actively with
host internal defenses, thereby assuring
continuation of the compatible association.
Natural resistance may result from the
host's ability to overcome both passive and
active processes employed by infecting
trematode larvae.
ACKNOWLEDGMENTS
Financial support has been provided by
NIH grants AI-16137 to C.J.B. and AI15503 to T.P.Y. We have profitted from
research and ideas of numerous colleagues,
most recently Sarah Fryer (Oregon State
University) and Michael J. Lodes (University of Oklahoma), to whom we express our
gratitude. We dedicate this paper to the
late Dr. Christopher A. Wright.
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