AMER. ZOOL., 29:1085-1093 (1989)
Symbiosis and Organismal Boundaries1
BETSEY DEXTER DYER
Department of Biology, Wheaton College,
Norton, Massachusetts 02766
SYNOPSIS. The functional boundaries of organisms may not be exclusive or discrete. The
genomes of organisms include not only stable genes which replicate faithfully at each
division but also transposable elements (jumping genes) and viruses which allow both
dynamic variability within a genome and interspecific genetic interactions. All organisms
(with the exception of specially maintained laboratory organisms) are in association with
other organisms. In close heterospecific associations (symbioses) there are selective advantages for mechanisms which enable organisms to coordinate their activities. In very close,
efficient symbioses, mechanisms to share the genetic control of essential, mutually used
structures, may have evolved via the activities of movable genetic elements (e.g., transposable elements). Interactions across species boundaries will include examples on the
genetic level, cellular level, and organismal level.
ing sensory functions for their hosts; (3)
This review paper is concerned with The theory of the endosymbiotic origins
questions about the definition of an indi- of eukaryotic organelles is briefly reviewed;
vidual organism and particularly considers and (4) Some of the extensive literature on
the importance of symbiosis in defining an the interspecific transfers of the genome is
discussed as it concerns the question of
organism.
One question to be considered is that of whether an organism is a functionally disthe physical boundaries of organisms. All crete entity.
organisms are contained within a cell memTHE BEHAVIOR AND PHYSIOLOGY OF
brane and many by more complex strucORGANISMS: A FUNCTION OF
tures such as cellulosic walls, exoskeletons,
and skins. Does the physical boundary
THEIR SYMBIONTS?
actually contain and define the true limitThere is a problem in defining a discrete
ing boundaries of an organism or can an physiology and behavior for an individual
organism somehow extend itself beyond organism. Axenic organisms (those lacking
these physical barriers?
symbionts) do not occur naturally. Thus,
A second question concerns the contents if one is taking symbiosis into considerof a membrane enclosed cell or (for exam- ation, experiments should include comple) a skin enclosed animal. To what extent parisons between "normal" symbiont-assoare the enclosed contents of an organism ciated organisms and axenic organisms. In
(the genes, enzymes, organelles) an entity the Animal Kingdom, axenic individuals
of independent existence (to paraphrase the are laboratory rarities, maintained with
Webster's dictionary definition of an great effort and cost. Also it would be
organism)?
extremely difficult to sort out by experiTo examine these questions the follow- mental design the influences of living coning topics (ranging from organism to cell ditions in an isolation cage versus living
to gene level) are reviewed: (1) The behav- conditions without symbionts, on the
ior and physiology of organisms are exam- behavior and physiology of an animal. In
ined within the context of their symbiotic other words the experiments have not been
associations; (2) Surface symbionts of done and may be nearly impossible to do.
organisms are considered as possibly hav- However, numerous observations may be
made of organisms and their symbionts in
their natural environments, and in many
1
From the Symposium on Is the Organism Necessary?
presented at the annual meeting of the American cases such observations indicate that the
Society of Zoologists, 27-30 December 1987, at New behavior and physiology of the same
Orleans, Louisiana.
organisms without their symbionts would
1085
INTRODUCTION
1086
BETSEY DEXTER DYER
be very different. The "wild-type" phenotype for certain behaviors and physiologies seems to be (in the following examples)
a function of the symbionts present.
Many marine fish, especially in the
deep sea, possess distinctive light organs
arranged in species specific patterns in and
on their bodies. It has been hypothesized
that the light organs are important to the
behavior of the fish. This has been demonstrated in Photoblepharon, the flashlight
fish, which seems to utilize its light organs
(positioned below its eyes) to detect and
lure prey, to avoid and possibly confuse
predators, and to communicate intraspecifically (Morin et al., 1975). The light
organs of this fish and of many other (possibly the majority) bioluminescent fish are
actually culture chambers filled with bioluminescent bacteria (Hastings and Mitchell, 1971; Morin et al., 1975;Dunlap, 1984).
Thus behaviors of vital importance such as
feeding, predator avoidance, and communication are a direct result of bacterial
symbionts. Although this has not been done
in the laboratory, the Gedanken-experiment may be imagined in which bioluminescent fish are deprived of their symbionts and the resulting behavior or lack
of behavior is observed. The bacteria are
an integral part of the functional and taxonomic entity that is defined as Photoblepheron. Without the bacteria, that definition
is incomplete or inaccurate.
Ruminant mammals are dependent upon
communities of microorganisms in their
digestive systems, to maintain their herbivorous, grazing life styles. The enzyme,
cellulase, which is necessary to break down
the plant material (mostly cellulose) is provided by some of the microorganisms
(Coleman, 1975). Termites also maintain
cellulolytic communities of microorganisms in their digestive systems. Laboratory
termites deprived of their symbionts (bacteria and protists) by antibiotic treatment
continue to eat wood but will starve to death
(Grosovsky and Margulis, 1982). Thus an
integral functional part of many cellulosedigesting macroorganisms, such as the
termites and ruminants, is actually a community of microorganisms. The mainte-
nance of their symbiotic community has
been an essential factor in termite evolution. Some specific aspects of termite
behavior such as proctodeal feeding (anus
to anus or mouth to anus) of newly hatched
nymphs or newly moulted instars, may have
evolved as a mechanism to re-establish the
symbiotic community lost during development (Wilson, 1971). Furthermore, the
social habit of termites, a major taxonomic
and behavioral characteristic, may have
evolved in response to the necessity of
maintaining the symbionts by passing them
from termite to termite (Cleveland et al.,
1934).
Researchers exploring the deep Pacific
Ocean trenches in the Alvin did not expect
to see large animals thriving so far below
the photic zone that sufficient photosynthetic products could not possibly be available to them. Yet, huge mollusks and giant
vestiminiferan worms were discovered in
the trenches near the outlets of hot, sulfide-rich springs. These organisms apparently live on carbon, fixed by chemoautotrophic bacteria which use hydrogen sulfide
as a source of energy and reducing power
(rather than sunlight and water). Some of
the animals, such as the giant vestiminiferan worms, maintain within their tissues
chemoautotrophic bacterial symbionts
which may be providing them directly (and
abundantly, given the size of the worm)
with fixed carbon (Cavanaugh etal., 1981).
The ability of these organisms to occupy a
particular niche which is rich in sulfides
(usually toxic to animals), low in oxygen,
and generally unavailable to photosynthesizers, probably depends upon their
chemoautotrophic bacteria. The distinguishing systematic characteristics of the
worms—the habitat, large size, and nutrition—seem to be a function of the symbionts (see also Reid, 1989).
Reef-building corals are distinguished
from solitary corals in several respects. The
reef builders are colonial and build up
extensive reefs composed of their calcium
carbonate exoskeletons. The solitary corals also have calcium carbonate exoskeletons but grow slowly and individually, never
producing reefs. The reef builders are in
SYMBIOSIS AND ORGANISMAL BOUNDARIES
the upper photic zone and the solitary corals are usually in the lower depths of the
photic zone. The reef builders maintain a
symbiotic community of photosynthetic
algae, zooxanthellae, while the solitary corals do not. It has been demonstrated that
the photosynthetic activity of the algae is
essential for the rapid precipitation of calcium carbonate necessary to build and
maintain reefs (as reviewed by Ahmadjian
and Paracer, 1986). An important taxonomic characteristic of reef-building corals—their ability to build reefs—distinguishing them from solitary corals is the
community of calcium carbonate-precipitating algae.
Many organisms maintain specific population levels of symbiotic photosynthetic
algae or the photosynthetic organelles of
algae in their tissues, as direct sources of
photosynthetic products (Muscatine and
Pool, 1979). Examples include the cnidarian, Hydra, the platyhelminth, Convoluta,
and the mollusk, Elysia (which maintains
chloroplasts) (reviewed by Ahmadjian and
Paracer, 1986). Some of the behaviors of
the animals such as basking in sunlight must
be a consequence of the animals' need to
maintain symbionts. Specialized tissues such
as the large flat dorsal mantle of Elysia
which contains neat agricultural rows of
chloroplasts, salvaged from Codium, are also
a consequence of the importance of the
symbiotic association.
Most terrestrial plants are associated with
mycorrhizal fungi in and on their roots.
The fungi may help plants to withstand
drought, high temperatures, and toxic
metals; they may enhance the transport of
water and minerals into the roots (reviewed
by Ahmadjian and Paracer, 1986). The fact
that mycorrhizal fungi are "endemic" to
terrestrial plants suggests their importance
as one of the evolutionary "adaptations"
for terrestrialization. Mycorrhizal fungi
grow not only in and on roots but extend
throughout the soil, and may thus act as
functional connectors between plants, both
inter- and intra-specifically. The consequences may be long distance networks of
associations between plants. One example
is the Indian Pipe, Monotropa, a parasitic
1087
plant which takes its nutrition from a
mycorrhizal basidiomycete fungus which
in turn receives nutrients from nearby tree
roots. Thus two plants are obligately linked
by the roots with a fungus, and the three
organisms together function as an entity.
Tapeworms have neither digestive systems, nor any apparent vestigial digestive
system. They do of course have the ability
to absorb nutrients through the integument. However tapeworms do require a
digestive system which they share with a
host organism. The loss of organs and
organ systems is the sort of evolutionary
streamlining expected in obligate symbionts. Just as viruses are not definable as
independent entities (being primarily
streamlined genomes dependent upon host
cells), an adult tapeworm virtually does not
exist apart from its host. The extent to
which it shares important functions with a
host leaves the tapeworm only nominally
defined as an individual.
All of these examples were selected
because the organisms have obvious major
behavioral and physiological functions
shared interspecifically. There may be far
more subtle and intricate associations binding organisms functionally together. Symbioses are the rule rather than the exception; organisms (outside of the laboratory)
are always associated with other organisms.
Bermudes and Margulis (1988) consider
symbiotic organisms to be like "semes"
(groups of genes coding for multigenic
traits) which are acquired evolutionarily by
organisms and are important in the subsequent evolution of organisms. A seme (or
symbiont) may help to define an organism
taxonomically, such as reef-building corals
with their symbiotic algae (as calcium carbonate-precipitating semes). A seme (or
symbiont) may select for specific tissue differentiation such as the special light organ
culture chamber of fish or loss of tissue
such as the loss of a digestive system by
tapeworms. In the case of the tapeworm
the seme that is being acquired is the collection of genes that codes for the entire
digestive system of the host organism.
Organisms as separate, completely definable entities may not exist. As I will show
1088
BETSEY DEXTER DYER
below cells as independent definable entities may not exist, and furthermore genes
may not be as intraspecifically faithful as
was once thought, with interesting consequences for evolution.
THE SENSORY SURFACE
Sieburth (1975) has published numerous
scanning electron micrographs of the surfaces of marine organisms. What is most
obvious from the micrographs is that the
surfaces are covered by bacteria, protists,
fungi, and small animals. Newly hatched
organisms are quickly colonized by surface
communities. The diversity of organisms
in a particular surface community seems to
be specific to the host. The micrograph of
the polychaete annelid, Nereis, is an anomaly in this collection of micrographs because
the organism appears to be completely
without surface symbionts. The question
to ask about Nereis is how does it maintain
this unusual condition and what selection
pressure for maintainance mechanisms
must there be in order to keep the surface
so clean? Communities of surface symbionts would seem to be the "normal"
situation for most macroorganisms.
Extremely dense coverings where no host
surface is visible seem to be typical for
organisms such as the amphipod Caprella
grahamii. Some questions to ask about these
organisms are (1) Do these surface communities serve any protective function? and
(2) What is the nature of an organism's
sensory neuron interactions with the environment through the blur of the surface
colonies? This section will examine the second question and will propose that some
surface layers of organisms may be acting
as sensory symbionts for their hosts, as
intermediates between the host and the
environment. They may even be transmitting specific information to the neurons or
sensory system of the host.
Cleveland and Grimstone (1964) first
described Mixotricha paradoxa, a large
trichomonad protist which lives as a symbiont in the hindguts of certain Australian
termites. M. paradoxa has four small motility organelles at the anterior end but the
rest of the large cell is almost completely
covered with at least two types of spiro-
chete bacteria and at least one type of rodshaped bacterium. The spirochetes have
been observed to move in synchrony propelling their host forward, thus acting as
motility symbionts. Since then, studies have
shown that many different protists of termite hindguts are associated with surface
bacteria. Some of the bacteria are motility
symbionts, while the function of others is
unknown. The intimate association of the
protist and its bacteria has been elucidated
with transmission electron microscopy (e.g.,
Breznak and Pankratz, 1977). In many
cases, the end of the spirochete is modified
to fit a differentiated insertion site on the
surface of the protist.
The initial idea that spirochetes and
other bacteria might also be acting as sensory symbionts for their hosts is based on
observations of preparations under light
microscope or of films of termite protists.
When a protist covered with bacteria (especially long, thin bacteria which extend from
the surface) comes in contact with another
protist or similar object the former protist
makes initial contact by means of its layer
of symbionts. Whether any information
about the contact is transmitted to the host
or not is unknown. Two items of circumstantial evidence support the hypothesis
that these bacteria are sensory symbionts:
(1) The intimate connection between host
and spirochete suggests that at least a physical mechanism for transmitting information might be possible. The force of contact of the unattached end of the spirochete
may cause a distinctive movement of the
attached end (sometimes inserted into a
socket) which could be perceived by the
host. (2) Transmission electron micrographs of some protists show a surface layer
of bacteria so dense that it is difficult to
imagine any direct contact of the host senses with the environment.
An interesting observation has been
made by Peter Beamish (Ceta Research
Inc., Newfoundland, personal communication; Beamish, 1986) concerning the
humpback whale Megaptera novianglia and
its associated barnacle Coronula diadema.
The barnacles, attacked to the fins and
other parts of the whale, are within 6-sided
exoskeletons. Beamish has determined that
SYMBIOSIS AND ORGANISMAL BOUNDARIES
1089
drial mutations conferring resistance to
antibiotics have been shown to recombine
(Thomas and Wilkie, 1968). Such recombinational events between mitochondrial
genes may be quite common in that mitochondria are frequently observed to be
undergoing fusions as well as reproductive
divisions. Mutations for antibiotic resistance also occur in plastid genomes of
Chlamydomonas and recombinational events
between plastid genomes may be observed
under certain laboratory conditions (Boynton etal, 1976). These independent genetic
WALKING COMMUNITIES OF BACTERIA
activities of mitochondria and plastids support
a rather dynamic model of" the genetic
The basic elements of the endosymbiotic
theory of the origins of eukaryotic cells will activity in a typical eukaryotic cell. A plant
be summarized here (for details see Mar- cell, for example, is a composition of at
gulis, 1981; Dyer and Obar, 1985). Specific least three types of formerly free-living
discussion will center on evidence for bacteria—the nucleocytoplasm host, the
genetic exchange between certain eukary- mitochondria and the plastids. Although
otic organelles—mitochondria and plas- these three are well integrated and coordinated temporally and spatially and
tids.
The endosymbiotic theory of the origins although they share the coding of many
of eukaryotic cells is that organelles of structures, the three component parts are
eukaryotes, mitochondria, plastids and genetically independent. The genetic
possibly motility organelles originated as products of the three components together
free-living bacteria which had entered into define the phenotype of the cell, and
symbiotic associations with a host bacte- recombination outside of the nucleus may
rium (ancestral to the nucleocytoplasm). contribute to changes in phenotype. A plant
Evidence for the hypothesis centers around cell is like an intimate community of bacthe autonomy and remnants of autonomy teria, coordinating their activities to profound in mitochondria and plastids (motil- duce the cell phenotype. Animals consistity organelles will not be discussed here). ing of millions or billions of cells, in which
Mitochondria and plastids are double- each cell is a symbiotic association of bacmembrane bounded organelles containing teria, may be thought of as highly coorDNA that codes for rRNA, tRNA, and dinated walking, swimming, or flying comsome of the mRNA needed to maintain munities of bacteria.
organelle structure and function. MitoMechanisms for gene exchange (some of
chondria and plastids have metabolisms which will be reviewed in the next section)
very similar to certain free-living bacterial may also be operating between the genomes
counterparts (for example Paracoccus and within eukaryotic cells. There is evidence
Prochloron). On this evidence, mitochon- that genes have been exchanged (via transdria and plastids are hypothesized to be posons or viruses?) between plastids and
former bacterial symbionts that are now mitochondria in corn (Stern and Palmer,
well-integrated organelles that have sec- 1984). Genetic exchanges between nucleus
ondarily lost some autonomy.
and mitochondria have been hypothesized
One specific aspect of plastid and mito- from observations that many structures in
chondrial autonomy is their ability to rep- mitochondria are coded for partly by the
licate and undergo genetic recombination. nucleus and partly by the mitochondria.
Mitochondrial mutants have been isolated There is further support for the hypothesis
from facultatively aerobic yeasts such as of gene transfer in observations that a parSaccharomyces cerevisiae, in which mitochon- ticular mitochondrial gene product found
drial function is not obligate. Mitochon- in fungi is coded for in the mitochondria
the skeletons have a particular acoustic
property—they can focus sound. These
6-sided exoskeletons are modified at the
base to accommodate folded outgrowths of
whale skin, forming an intimate whale-barnacle connection. As the barnacle feeds on
phytoplankton it makes clicking sounds,
which are enhanced and transmitted by the
exoskeleton. Beamish hypothesizes that the
whale may be using the barnacle clicks to
echo-locate small fish, the whale's probable
prey.
1090
BETSEY DEXTER DYER
in some fungi, and in the nucleus in others
(van den Boogart et ai, 1982).
Thus, in addition to the "intraspecific"
genetic autonomy of cell organelles, there
may be considerable "interspecific" genetic
exchange within cells. A eukaryotic cell may
be considered to be the phenotypic result
of a network of genetic exchanges. This
does not support a clear-cut definition for
organisms, but is consistent with the theme
of this paper—that the boundaries between
organisms may be blurred by close symbiotic associations.
THE UNFAITHFUL GENOME
The image of the genome as a stable
entity, replicating faithfully generation
after generation, is less and less well-supported by the growing body of evidence
from molecular geneticists concerning the
activities of genes. In fact, given the number of mechanisms (plasmids, viruses,
transposons) by which genes can rearrange
themselves and be rearranged, it might
seem remarkable that a genome is replicated with any fidelity at all. That there is
considerable fidelity is an attribute of
mechanisms such as DNA repair, precision
mitosis and meiosis, cellular defenses
against foreign genomes, and organismal
defenses against hybridization, which
maintain a significant degree of genomic
integrity within an organism. These mechanisms manage quite effectively to prevent
a completely free-flowing, interspecific
exchange of genetic information which
would tend to obliterate distinctions
between organisms. Mayr (1982) recommends that in defining species, it would be
better not to focus on messy situations such
as the common occurrence of "leakage" in
plant isolating mechanisms which result in
interspecific hybridization. Mayr supports
the idea of the general reliability of the
species specificity of genomes as the focal
point in defining species. In fact, the most
conservative definition of a species (most
useful for sexual animals in which full
reproductive cycles may be observed) is that
organisms of the same species are exclusively interfertile and produce interfertile
offspring. While this helps somewhat to sort
out the classification of horses and don-
keys, it is too strict to be applied to organisms which are non-sexual or which cannot
be observed through a reproductive cycle
or which (for example) have leaky isolation
mechanisms. In the following section, the
contrary idea will be developed—that it
may be very useful to focus on the numerous interspecific genetic exchanges and to
consider the implications for the evolution
and the identity of organisms.
There may be strong selection pressures
for organisms in symbiotic association to
exchange genes and to maintain those
genes that have been acquired. Dyer and
Obar (1984) propose a sequence of steps
by which a symbiotic association becomes
"more obligate" by becoming more efficient. A first step would be a symbiosis
in which two heterospecific organisms
exchanged nutrients in such a way that the
association is of selective advantage, in that
the two organisms together leave more offspring than the independent individuals.
In the next steps, there are selection pressures for ensuring that the partners do not
outgrow each other, mechanisms which
might include coordination of respiratory
rates and cell division. This could be
accomplished initially by the development
of enzymatic controls by each partner over
the other. In further steps, the selection
pressures might be loosened for the maintenance of non-functional or redundant
genes and their products.
For example, an endosymbiont may no
longer need a protective cell wall. A particular enzyme produced by both partners
might be lost in one partner. In very refined
and efficient symbioses, the coordination
of partners is on the genetic level. Selection
would be for the coordinated coding of
important gene products, and a loss of
autonomy for both partners. This could be
accomplished via naturally occurring gene
transfer mechanisms, and could result in
situations such as that of mitochondria and
their host eukaryotic cell. The major mitochondrial ATPase of mitochondria has
multiple subunits, some of which are coded
by the mitochondria and some of which
are coded by the nucleus. It has been suggested that all of the subunits originated
as mitochondrial products (Obar and
SYMBIOSIS AND ORGANISMAL BOUNDARIES
Green, 1985). Coordinated coding provides a selective advantage in that it helps
ensure coordinated growth of the partners
and facilitates development of an obligate
relationship. The next step in the integration of heterospecific partners is perhaps
the most difficult to document—the centralization of the genome. In a symbiotic
association ultimate genetic efficiency could
be visualized as the maintenance of the two
partner genomes as one large coordinated
genome. Once such an event had occurred,
it would be difficult to trace its past. Is it
possible to tell apart a single independent
genome from a well-integrated genome
composed of the two sets of genes of two
partners? The tendency toward centralization may be observed in mitochondria
which seem to have donated most of their
genes to the centralized nucleus. While
gene transfer mechanisms generally do not
seem to be unidirectional, there is currently no evidence of transfer from nucleus
to mitochondria. The apparent unidirectionality may be the result of the means by
which genes are passed on cell to cell. The
single centralized nucleus is almost guaranteed to pass a copy of the genome to each
daughter cell. A single mitochondrion, one
of about 50 in the cell, is less likely to send
an offspring mitochondrion into each of
the offspring cells and is thus less likely to
be able to preserve the results of a gene
transfer event. The centralized genome is
most likely to transfer advantageous new
arrangements of genes and is most likely
to assure the coordination and integration
of the partners.
Plasmodium, the malaria parasite, has
evolved several mechanisms by means of
which it controls its host cell's enzymes and
activities. The degree to which Plasmodium
and host have integrated their activities is
illustrative of the initial steps in efficient
establishment of symbioses. Plasmodium
does not enter red blood cells by any direct
activity of its own. It binds to red blood
cells and alters host cell membranes in such
a way that the host cell invaginates and
takes in the parasite (Bannister, 1979).
Under the control of the parasite, the host
cell actively responds thereby causing the
invasion of the parasite. Once inside the
1091
red blood cell, Plasmodium berghei does not
use its own superoxide dismutase but
apparently takes up the host superoxide
dismutase for its own use (Fairfield and
Meshnick, 1983). Plasmodium also does not
produce its own glucose-6-phosphate dehydrogenase. Evidence for this is the fact that
human hosts with a deficiency in the
enzyme cannot maintain the parasite. Thus
Plasmodium has lost some redundant or
"unnecessary" genes and has evolved
mechanisms to use host products instead.
Most leguminous plants are in symbiotic
association with nitrogen-fixing bacteria,
maintained by the plants within root nodules. The establishment of the symbiosis is
the result of the coordinated activities of
both partners. Beringer et al. (1979)
describe a particular Rhizobium entering an
association with a legume. The Rhizobium
penetrates the root cell with an infection
thread, stimulating plant cell division. The
dividing host cells help to distribute the
Rhizobium in the root. High levels of plant
hormones, probably synthesized by the
bacteria, stimulate formation of protective
root nodules (as reviewed in Beringer et al.,
1979). Bacteria within the cells of the root
nodules grow larger and more rounded.
Nitrogenase, the enzyme with which Rhizobiumfixesnitrogen, is sensitive to molecular oxygen. In the protected nodule, a
type of hemoglobin is produced which
removes free oxygen from the environment of nitrogenase. The heme of the
hemoglobin is coded for by the bacteria
and the globin is coded for by the plant—
a striking example of coordinated coding
for a product (Cutting and Schulman, 1971;
Roberts, 1981).
Rahat (1987) hypothesizes that the cnidarian Cassiopeia andromeda may have lost
one or more genes and literally cannot
complete a life cycle without receiving particular metabolites supplied by symbiotic
bacteria.
Agrobacterium, a symbiont of plants,
makes an intimate genetic association with
its host. The bacteria carry plasmids which
are transferred to the host cells and which
become integrated into the host genome.
The host cell transcribes and translates the
plasmid genes producing unusual amino
1092
BETSEY DEXTER DYER
acids called opines, that are not used by the
plant but are taken up as nutrients by the
bacteria. The bacteria also stimulate cell
division at the site of injection, resulting
in tumor-like growth (Chilton, 1983; as
reviewed by Ahmadjian and Paracer,
1986).
Jeon has been following an interesting
example of genetic integration between
symbionts (Lorch and Jeon, 1981; Jeon,
1983; Reisser et al., 1985). Amoeba proteus
in culture suddenly became infected with
large numbers of bacteria, up to 150,000
bacteria per ameba. Infected amebae were
maintained with great care and observations were made for 20 years on the nature
of the association. It was noticed that
adverse effects lessened eventually and that
after several years the host ameba had
evolved a dependence on the bacteria. It
was found through nuclear transplant
experiments that nuclei from infected
amebae would no longer "support" uninfected amebae, as though some gene had
been lost or changed in the association.
Treatment with antibiotics resulted in
death of the symbiotic amebae, but they
could be rescued with more bacteria. Jeon
(1987) calls the bacteria "quasi organelles." Several proteins produced by the
bacteria may be found in the host cytoplasm although functions of the proteins
are unknown. It may be that these or other
proteins produced by the bacteria are now
a necessity for this newly evolved strain of
amebas.
Sonea and Panisset (1983) propose a fascinating hypothesis which will be only
briefly mentioned here. They propose that
mechanisms for gene transfer are so widespread and commonplace among bacteria
that there is actually a "genetic unity" in
bacteria. They suggest that in nature, bacteria theoretically have access to the genes
of all of the other bacteria. Given the
colonial evolutionary history of eukaryotes, this hypothesis may have consequences for our understanding of eukaryotes as well.
CONCLUSIONS
On the genetic level, the cellular and
tissue levels, and the whole organism level,
there are many means by which traditionally defined boundaries of organisms may
be crossed. There may in fact be strong
selection pressures for crossing these
boundaries, centered primarily on the
maintainance of intimate symbiotic associations between heterospecific organisms.
The evolutionary consequences may be
enormous, encompassing not only communal origins of cellular components, but
even communal phenotypes of animals and
plants. Organisms are part of a continuum
in both space and time; their boundaries
reach as far as the point at which one
organism no longer influences another.
The title of this symposium was "Is the
organism necessary?"; the answer from the
point of view of this paper is "Yes, all of
them."
ACKNOWLEDGMENTS
Lynn Margulis, Robert Obar, David Bermudes and students in my 1987 Cell Biology class at Wheaton College discussed
some of these topics with me. Some ideas
were generated by ideonomical techniques
(Patrick Gunkel, Austin, Texas). Ideonomy is the study of and generation of ideas.
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(Megaptera novianglia). Abstract. N.E. Marine
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Beringer, R. E., N. Brewin, A. W. B.Johnston, H. M.
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