Download Animal-Bacterial Interactions in the Early Life History of Marine

AMER. ZOOL., 34:554-561 (1994)
Animal-Bacterial Interactions in the Early Life
History of Marine Invertebrates:
The Euprymna scolopesIVibrio fischeri Symbiosis1
MARGARET J. MCFALL-NGAI
University of Southern California, Department of Biological Sciences, Los Angeles, California 90089-0371
SYNOPSIS. The symbiotic association between the Hawaiian sepiolid squid
Euprymna scolopes and the marine luminous bacterium Vibriofischeriis
being developed as a model system for the study of animal-bacterial
interactions during development. Changes in light organ morphology during embryogenesis foster successful infection of the light organ with the
proper bacterial partner. These embryonic events of light organ morphogenesis include the elaboration of an epithelial surface with a complex
ciliated, microvillous field. The squid host hatches without the bacterial
symbionts, but acquires them within hours from the free-living population
of the bacteria in the water column. Upon exposure to the proper symbionts, the host organ undergoes a series of morphogenetic changes,
including loss of the ciliated, microvillous field. The light organ then goes
on to mature into a morphological configuration that serves to promote
the maintenance of a stable association with the bacteria and that correlates with the use of the bacterial bioluminescence in behavior of the
host. This symbiosis is discussed in light of other cyclically transmitted
animal-bacterial associations.
INTRODUCTION
A growing database exists suggesting that
many marine invertebrate larvae and juveniles incorporate bacteria into specific stages
of their development (see e.g., Zimmer and
Woollacott, 1983; Hofmann and Brand,
1987; Gil-Turnes et al, 1989; Walker and
Lesser, 1989; McFall-Ngai and Ruby, 1991;
Bosch, 1992). In this contribution, I explore
some areas of animal-bacterial interactions
that should be relevant to the future study
of the role of such associations in animal
development. In addition, I review aspects
of recent research on the symbiosis between
the sepiolid squid Euprymna scolopes and
the marine luminous bacterium Vibrio fischeri, which is an emerging, experimental
model system for the study of the establishment and maintenance of stable animalbacterial cooperative associations.
SPATIAL AND TEMPORAL PATTERNS OF
ANIMAL-MICROBIAL INTERACTIONS
The intimacy of the relationship
All aspects of the relationship between
animals and microbes will be affected by
the physical, spatial relationship that the
microbe has with the cells of the host. Traditionally, biologists have categorized
microbial symbionts as being either extracellular or intracellular (Smith and Douglas,
1987). Extracellular microbial partners can
occur, depending on the symbiosis, over a
spectrum of topographical locations in which
they are anywhere from superficial to
invested deeply in microvilli of specifically
evolved symbiotic tissues. Intracellular
microbes occur either inside vacuoles or free
in the host cytoplasm.
Recent research on the mobility of DNA,
often referred to as horizontal gene transfer
{e.g., transposition, plasmid translocation),
has revealed mechanisms for the direct
interaction
between the DNA of two unre1
From the symposium Evolutionary Morphology of lated organisms (Doolittle et al., 1990;
Marine Invertebrate Larvae and Juveniles at the Annual
Meeting of the American Society of Zoologists, 27-30 Amabile-Cuevas and Chicure, 1992; Smith
et al, 1992). Thus, we must now include in
December 1993, at Los Angeles, California.
554
THE EUPRYMNA/VIBRIO
an equation considering the spatial relationship of the cells of the partners not only
how the entire host cell interacts with the
entire microbial cell, but also how the
genomes of the two organisms may physically communicate; i.e., this communication can be mediated by intervening cascades of biochemical messages mediated at
the membranes where two cells interface
(Fisher and Long, 1992), or through direct
intercalation of the foreign DNA into the
host or symbiont (Chilton, 1983). Further,
any given symbiosis may include, in either
its evolution or its ontogeny, extracellular
and intracellular stages, as well as indirect
and direct interaction with the foreign
genome.
These complex levels of spatial interaction will define how changes in gene expression in host and microbe are achieved in
the symbiosis. Such processes are currently
best understood in several well studied plantmicrobial symbioses. The early stages of the
root-nodule symbiosis between nitrogenfixing rhizobia and leguminous plants are
extracellular, while later stages are intracellular (Fisher and Long, 1992;Hirsch, 1992).
In contrast, in the classic example of horizontal gene transfer, the extracellular symbiont Agrobacterium tumifaciens transfers a
plasmid to the host genome of a dicotyledonous plant (Chilton, 1983; Zambryski et
al., 1989). This plasmid contains genes that
encode enzymes which function to convert
host primary metabolites to opines, substances that cannot be metabolized by the
host. The opines are translocated to the bacterium, providing the microbial symbiont
with a well balanced complement of nitrogen- and carbon-rich biomolecules. Further, other genes carried on the plasmid contribute to the mechanism by which the
bacterial parasite promotes the transcription and overproduction of host hormones,
thereby causing hyperplasia in the plant and
the eventual formation of the mature gall.
In contrast to these plant-bacterial symbioses, the development of animal-bacterial
symbioses has not been well studied. Thus,
the possible roles that the spatial relationships and the degree of genomic exchange
between the two partners play have not been
explored extensively. Nevertheless, there is
SYMBIOSIS
555
some evidence that genetic exchange can
occur between bacterial symbionts and heterotrophic hosts. For example, gene
sequence comparisons have provided strong
evidence for the acquisition by the prokaryotic enteric symbiont Escherichia coli of a
eukaryotic glyceraldehyde-3-phosphate
dehydrogenase gene (Doolittle et al., 1990),
and for the acquisition by the eukaryote
Entamoeba histolytica of a prokaryotic iron
superoxide dismutase gene (Smith et al.,
1992). Thus, evidence for genetic exchange
in development of any organism does formally exist.
Transmissionfrom generation to generation
The development of the above-described
spatial relationships during the life history
of the host are, to a large extent, determined
by the mechanisms by which the symbiosis
persists from generation to generation. Two
different modes are recognized: transovarian and cyclic, with cyclic transmission being
the more commonly occurring (Douglas,
1987; Dyer, 1989; Saffo, 1992). In transovarian transmission, the symbionts are
passed from adult to progeny in, or on, the
egg {e.g., insect "mycetocyte" symbioses;
Douglas, 1987). Thus, the microbes are
incorporated into the events of embryogenesis and are considered "self; i.e., they are
present as a component of the animal during
the developmental period when non-self
recognition mechanisms are established. In
contrast, cyclic transmission occurs when
the animal acquires its microbial symbiont
from the environment as a larva or juvenile;
i.e., the microbe is not directly included in
events of embryogenesis. In those associations where the microorganisms are rare in
the environment, behaviors have evolved
in the adult host which facilitate the transfer
of symbionts to the juveniles via the enteric
tract [e.g., ruminants (Coleman, 1975); termite (Wilson, 1971)]. Often, however, the
symbiont is a common component of the
environmental microbiota and is acquired
by the juvenile without a direct interaction
with the adult host [e.g., non-ruminant
mammalian intestinal microbes (Smith and
Crabb, 1961); zooxanthellae (Muscatine and
Porter, 1977); luminous bacteria of squid
and fish light organs (McFall-Ngai, 1991;
556
MARGARET J. MCFALL-NGAI
McFall-Ngai and Ruby, 1991; Haygood,
1993); the vent tube worm Riftia pachyptila
(Caryetal., 1993)].
in response to dietary changes during ontogeny (Smith and Crabbe, 1961).
In the case of cyclic transmission, inter- THE EUPRYMNA SCOLOPES-VIBRIO FISCHERI
SYMBIOSIS AS A SYSTEM FOR THE STUDY
actions between the host and symbionts
OF THE CYCLIC TRANSMISSION OF
occur stepwise in two distinct temporal
BACTERIAL SYMBIONTS
phases: 1) preparation before the initiation
of the relationship; and, subsequently, 2)
While most, if not all, animals have speevents triggered by the first direct interac- cific associations with microbes, this area
tions. In the first phase, the host expresses of biology has been little studied, largely due
a developmental program that results in a to the absence of a technically feasible model
population of the cells poised to interact system. Many animals are known to harbor
with specific, appropriate microorganisms essential microorganisms in their gastroinin the environment; e.g., specific receptors testinal tracts, but usually they exist as a
must be in place to ensure that the proper dynamic consortium of numerous interactrelationship is fostered. The second phase ing species (Smith and Crabbe, 1961). Thus,
encompasses those responses on the part of in experimental studies, it is not possible to
both the host and the symbiont that occur distinguish the influence of any one species
as a result of their direct interaction. The on the community as a whole. In other cases,
interactions during this phase mediate the such as the symbiosis between chemoaudevelopment of the "active" symbiotic state, totrophic bacteria and various marine
in which genes or gene products are ulti- invertebrates (Childress and Fisher, 1992),
mately translocated between partners.
where the symbiosis is characteristically one
Often these two phases correspond to the host and one microbial species, the host
embryonic and postembryonic periods of organisms either are rare, or one (or both)
development. However, in animals such as of the partners cannot be raised indepenmarine invertebrates with complex life his- dently under laboratory conditions. Furtories involving larval stages, the interac- ther, in many symbioses that have been
tions can occur exclusively at distinct and studied thus far, pivotal in the relationship
specific time periods in the life history after is the derivation of nutrients from the
hatching. For example, in the alternation of microbial component. Separation of the
generations of the scyphozoan Cassiopea sp., partners results in a state of compromised
metamorphosis of the planula larva requires health for the host animal (Gordon and Pesti,
an interaction with ambient seawater bac- 1971; Nardon and Grenier, 1989).
teria (Hofmann and Brand, 1987), and the
The symbiotic association between the
maturation of the medusa also depends upon sepiolid squid Euprymna scolopes and the
interactions with the zooxanthellae (Trench gram negative luminous bacterium Vibrio
et ai, 1981). Recently it has been reported fischeri offers several advantages as a system
that specific bacteria associate with the sur- for the study of cooperative interactions
faces of the larvae of some shrimp (Gil- between bacteria and animals (McFall-Ngai
Turnes et al, 1989) and lobster (Gil-Turnes and Ruby, 1991; Ruby and McFall-Ngai,
and Fenical, 1992) species. These associa- 1992). The host is a relatively abundant
tions are believed to be obligate in nature, inhabitant of the shallow sandflatsof Hawaii
because the microbe produces an antifungal (Singley, 1983), and the bacteria occur not
compound that serves to protect the larvae. only as symbionts with the squid, but also
In addition, although the author is not aware as free-living components of the bacterioof any studies on the subject, the essential plankton (Lee and Ruby, 1992). The symgut microbiota of marine invertebrate lar- biosis that has evolved between these two
vae may vary from stage to stage as diet organisms consists of one host and one bacchanges, in much the same way as the essen- terial species, both of which are culturable
tial microbiota of the mammalian infant is outside of the symbiosis. The host provides
considerably different than that of the adult a nutrient-rich environment for this hetero-
THE EUPRYMNA/ VIBRIO SYMBIOSIS
537
FIG. 1. A significant portion of the Euprymna scolopes life cycle involves development and maturation of the
light organ system. Mature females lay eggs that hatch after approximately 20 days (A). During this embryonic
period, the light organ develops those tissues that will ensure inoculation of the organ with symbionts. At
hatching, the light organ bears superficially a ciliated, microvillous epithelium with three pores (upper left figure,
left half). The pores lead to three independent crypts deep in the organ (upper left figure, right half). Upon
exposure to symbiosis-competent Vibrio fischeri, the light organ undergoes a morphogenetic process over an
approximately 5 day period (B) that results in the loss of the superficial structures, coalescence of the three pores
into one (upper middle figure, left half), and enlargement of the crypts to accommodate the growing culture of
symbionts (upper middle figure, right half). Further maturation of the light organ over the next several weeks
(C) results in a mature light organ that maintains a stable association with the symbiont. During this period,
the tissues associated with the behavioral use of the bacterial bioluminescence are elaborated. Scale bars on the
figures representing the juvenile light organs = 100 microns; scale bar on the figure of the mature light organ =
1 mm.
trophic bacterium, and the host derives
luminescence (rather than a nutritional benefit) from the culture of approximately 1
billion bacteria that live in the extracellular
epithelial crypts of the light organ.
While experimental data on the bioluminescent behavior of the squid are few
(Moynihan, 1983), the morphology of the
light organ suggests that the bacterial light
is used in predatory and antipredatory
behavior of the squid (McFall-Ngai and
Montgomery, 1990). The mature light organ
consists of a core of epithelial tissue that
occurs as narrow crypts within which are
housed the bacterial symbionts (Fig. 1;
McFall-Ngai and Montgomery, 1990). The
epithelial cells are strongly polarized, and
their apical surfaces show elaborate, lobate
microvilli that invest the extracellular bacterial cells. The crypts communicate with
the mantle cavity through two pores, one
on each lateral face of the mature light organ.
Surrounding much of this epithelial-cell core
is a thick reflector which is itself surrounded
by the ink sac. The ink sac covers the entire
dorsal surface of the light organ. The amount
of light emitted by the light organ into the
environment is controlled by the dynamic
behavior of diverticula of the ink sac in much
the same way that the ocular iris controls
the amount of environmental light admitted
into the eye. Finally, the entire ventral surface of the light organ is covered by a transparent, muscle-derived lens (Montgomery
and McFall-Ngai, 1992; Weis et al, 1993).
These components of the light organ system
558
MARGARET J. MCFALL-NGAI
FIG. 2. Scanning electron micrographs of the light
organ of the juvenile Euprymna scolopes. The top panel
is the light organ of a newly hatched juvenile; the bottom panel is the light organ of a juvenile after a few
days of symbiosis with Vibriofischeri.Scale bar = 100
microns.
are thought to work in concert to effect
counterillumination behavior; i.e., emission of a ventral glow that is of the same
quality as downwelling light, and thus camouflages their silhouette from predators
below (McFall-Ngai, 1990, 1991).
The persistence of the Euprymna-Vibrio
relationship between generations is mediated through a process of cyclic transmission. Female squid lay between 50 and 400
fertilized eggs in each of a series of clutches
placed on hard substrates, such as the rocks
and coral rubble associated with the backreef habitats where the squid are abundant.
After an embryonic period of approximately 20 days, the juvenile squids hatch.
Within hours of hatching, the incipient
symbiotic organ of the juvenile becomes
colonized by planktonic V. fischeri (Ruby
and Asato, 1993).
Distinct morphological and anatomical
features characterize both the initiation
phase and the subsequent maintenance
phase of the interaction between squid and
the bacteria (Fig. 1). During embryogenesis,
the squid develops tissue that has been
selected over evolutionary time to be competent to interact only with the V. fischeri
cells present among the bacterioplankton in
the ambient seawater. The "conversation"
between the two partners during this initiation phase must be such that only V. fischeri colonizes the symbiotic organ. At
approximately 100 cells/ml, V. fischeri
occurs as only about 0.001% of the bacteria
in the water column (K. H. Lee, personal
communication). In the few days following
successful colonization of the light organ,
this structure "metamorphoses" into an
organ whose primary function is the maintenance of the symbiotic state (Figs. 1 and
2; McFall-Ngai and Ruby, 1991; Montgomery and McFall-Ngai, 1994). The complex
changes in morphology of both the host and
the symbiont that occur during this period
suggest an intimate dialogue between the
partners.
The exact biochemical and genetic nature
of this early dialogue between host and symbiont has yet to be elucidated. However,
early studies have revealed some interesting
features of the light organ system that have,
in turn, suggested some avenues for future
investigation. In the absence of symbiosiscompetent strains of V. fischeri, the light
organ remains uncolonized by any other
bacterial species. This observation suggests
that V.fischeridoes not simply outcompete
other bacteria for a habitat that would be
suitable for a wide variety of bacteria.
Instead, either specific recognition events
mediate infection, or the light organ creates
an environment where only symbiosiscompetent V. fischeri can persist; alternatively, some combination of both of these
possibilities may exist. Preliminary data
suggest that recognition may be partially or
wholly mediated by lectin-glycan interactions between the host and symbiont (Weis,
Brennan, and McFall-Ngai, unpublished
data). Further, characterizations of the light
THE EUPRYMNA/VIBRIO
organ indicate that the animal may create
a stressful environment in which only the
proper symbiont can persist (Weis et ai,
1992; Tomarev et al, 1993).
SYMBIOSIS
559
divisions in the underlying mesenchyme
layer. Over the last half of embryogenesis,
two distinct areas of the embryonic light
organ are elaborated—a set of superficial
structures, and a set of pockets or crypts.
The superficial structures consist of complex ciliary, microvillous fields (Fig. 2).
Thesefieldsoccur on each of the lateral faces
of the incipient light organ in two forms: (i)
a pair of two ciliated, microvillous epithelial
appendages (CEA), one anterior and one
posterior, and (ii) an area that extends out
from the base of these structures. At the base
of the CEA, on each of the two sides, are
three pores that lead to three epithelial-lined
pockets or crypts; i.e., the light organ at
hatching has a total of 6 pores, leading to 6
non-connected crypts. The crypts form
sequentially during development, with the
first beginning to form about % of the way
through embryogenesis and the last of the
three beginning to form only a couple of
days before hatching.
Embryonic development of the light organ:
Selection for tissues that mediate
colonization
In the case of most invertebrate larvae,
special structures for the handling of the
establishment and maintenance of mature
interactions with microbes have not evolved
without precursors. Instead, already existing structures have been co-opted, that may
be otherwise available throughout the life
history in relatives, but are lost in the mature
symbiosis. For example, Riftia pachyptila,
the vent tube worm, has a transient mouth,
through which the symbionts are presumably introduced during the inoculation process at each generation (Jones and Gardiner,
1989). In these cases, it may be difficult to
discern those processes that are involved in
initiation of the symbiosis from those that
are vestigial. The Euprymna-Vibrio sym- The functional morphology of the
biosis, however, is the only recognized juvenile light organ
example in which structures are present
In the hatchling, the light organ is located
whose sole function may be to insure the in the posterior portion of the funnel. Thus,
inoculation of the appropriate symbiont. much of the water that is brought into the
However, it should be noted that it is quite mantle cavity during ventilation passes
likely that other such structures will be found across the surface of the juvenile light organ
in related sepiolid-bacterial symbioses (Montgomery and McFall-Ngai, 1993).
(Pierantoni, 1918). In E. scolopes these When the animal is anesthetized, the chrostructures respond dramatically to interac- matophores become punctate rendering the
tions with the symbiont (see below). Thus, animal nearly transparent. Under these conwhile the presence of such structures is
unusual to symbioses, it offers the unique ditions, the CEA on the juvenile light organ
opportunity to study the developing inter- can be seen to form a ring, with the tips of
actions between a host tissue and its sym- the anterior and posterior appendages combionts, without the confounding influences ing in close apposition (Fig. 1; McFall-Ngai,
of any non-symbiotic functions of that tis- personal observation). Dissection of the light
organ from the anesthetized juvenile does
sue.
not appear to alter the configuration of the
components of the organ. Preliminary highEmbryonic development of the Euprymna
speed cinematographic studies of the juvescolopes light organ
nile organ have revealed that movements
The development of the E. scolopes light of the cilia entrain water particles around
organ system, and the structures associated the vicinity of the light organ (Emlet and
with the inoculation process, begins approx- McFall-Ngai, unpublished data).
imately halfway through embryogenesis in
Upon colonization with V. fischeri, the
the area of the nascent hindgut-ink sac com- light organ undergoes a dramatic metamorplex (Montgomery and McFall-Ngai, 1993). phosis (Fig. 1). Over a period of four to five
First apparent is a lateral thickening of this days, the ciliated, microvillous field is lost
region that appears to be the result of cell (Fig. 2), at least partially through the process
560
MARGARET J. MCFALL-NGAI
of cell death (Montgomery and McFall-Ngai,
1994). In addition, the three pores on each
side of the light organ coalesce into one single pore. Further, the volumes of the light
organ crypts enlarge, primarily by an
increase in the volumes of the epithelial cells
lining the crypts. These changes in the light
organ do not occur if the symbiont is withheld. In the absence of experimental genetics in these squids, such as that available in
Drosophila, to select for a juvenile without
CEA, it is difficult to prove definitively that
the CEA function in the colonization of the
light organ with V. fischeri. However, their
disappearance upon infection is strong correlative evidence that they are involved in
the successful colonization of the juvenile
light organ.
CONCLUSIONS
In the squid-luminous bacteria symbiosis
the exact biochemical and molecular mechanisms underlying the establishment of the
association remain to be elucidated. In the
broader view, however, there exists a wide
variety of interesting questions that pertain
to the role of bacteria in invertebrate larval
development. These include: (i) which of
the marine invertebrate larvae associate
with, or require for metamorphosis, specific
microbiota?; (ii) in those that have such a
requirement, what is the nature of the interaction?; and, (iii) similarly, how does the
microbial complement change with each
successive larval stage?
ACKNOWLEDGMENTS
I thank R. Emlet and E. Ruppert for the
invitation to participate in this symposium.
E. Ruby made invaluable suggestions on the
manuscript. I am grateful to the faculty and
staff of the Hawaiian Institute of Marine
Biology, University of Hawaii, who have
provided field support in the development
of these studies. The research on the squidbacterial mutualism discussed in this paper
is funded by NSF grant #IBN 9220482 and
ONR grant #N00014-91-J-1357 to the
author. HIMB Contribution number 938.
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