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Applied and Environmental Microbiology, August 2000, p. 3550-3555, Vol. 66, No. 8
0099-2240/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Temperature Affects Species Distribution in
Symbiotic Populations of Vibrio spp.
Michele K.
Nishiguchi*
Department of Biology, New Mexico State
University, Las Cruces, New Mexico 88003-8001
Received 17 March 2000/Accepted 13 May 2000
 |
ABSTRACT |
The genus Sepiola (Cephalopoda: Sepiolidae) contains 10 known species that occur in the Mediterranean Sea today. All
Sepiola species have a light organ that contains at least
one of two species of luminous bacteria, Vibrio fischeri
and Vibrio logei. The two Vibrio species
coexist in at least four Sepiola species (S. affinis, S. intermedia, S. ligulata, and
S. robusta), and their concentrations in the light organ
depend on changes in certain abiotic factors, including temperature.
Strains of V. fischeri grew faster in vitro and in
Sepiola juveniles when they were incubated at 26°C. In contrast, strains of V. logei grew faster at 18°C in
culture and in Sepiola juveniles. When aposymbiotic
S. affinis or S. ligulata juveniles were
inoculated with one Vibrio species, all strains of V. fischeri and V. logei were capable of infecting both
squid species at the optimum growth temperatures, regardless of the squid host from which the bacteria were initially isolated. However, when two different strains of V. fischeri and V. logei were placed in direct competition with each other at either
18 or 26°C, strains of V. fischeri were present in
sepiolid light organs in greater concentrations at 26°C, whereas
strains of V. logei were present in greater concentrations
at 18°C. In addition to the competition experiments, the ratios of
the two bacterial species in adult Sepiola specimens caught
throughout the season at various depths differed, and these differences
were correlated with the temperature in the surrounding environment. My
findings contribute additional data concerning the ecological and
environmental factors that affect host-symbiont recognition and may
provide insight into the evolution of animal-bacterium specificity.
| |
INTRODUCTION |
The existence of symbiotic
associations between eukaryotic hosts and microbial partners has long
intrigued biologists (1, 8, 9). The diversity and broad
range of each host-symbiont pair demonstrate how each partner has
coevolved to exploit new ecological niches and to provide a new
capability or function for the newly adapted individual or population
(10, 25, 34). Although a number of symbiotic partnerships
have evolved as parts of adaptations to particular ecological niches,
there has always been the question of whether the ecology or the
specificity of the partnership drives the evolutionary radiation of the
hosts and their symbionts. Do environmental factors contribute to the evolution of independent populations that eventually leads to speciation? If a preference exists between a symbiont and a host, how
is specificity maintained in associations in which the partnership is
either promiscuous or environmentally transferred?
Studies investigating the nature of symbiotic associations are
beginning to answer some of these questions and to provide clues to the
underlying mechanisms of host-symbiont cospeciation (11, 15, 16,
26). One example that is shedding light on the evolutionary
history of symbiotic associations is the partnership between a group of
shallow-water benthic squids (family Sepiolidae) and their luminous
bacterial symbionts (genus Vibrio) (22, 23). This
system has provided molecular and physiological evidence for the
coordinated influence of bacteria on the parallel evolution and
specificity of closely related host species (20, 31). Until
recently, all luminous bacterium-animal mutualisms were thought to be
monotypic; i.e., it was thought that only one species of bacterium was
associated with a particular host taxon (27, 33). However,
Fidopiastis et al. (12) discovered a new species of luminous
bacteria that resides in the light organs of several species of
Mediterranean sepiolid squids (genus Sepiola), which results
in a two-species consortium (21) (Vibrio fischeri
and Vibrio logei). This unique and interesting finding is
the first observation of two luminous species of bacteria residing in
the light organs of sepiolid squids. What is peculiar about the
two-symbiont relationship is that the two Vibrio species
differ not only in their 16S ribosomal DNA (rDNA) genotypes but also in
some of their physiological characteristics (12). Most
notably, the in vitro growth rates of V. logei
isolates are higher than the in vitro growth rates of V. fischeri isolates at lower temperatures (18°C), whereas at
higher temperatures (26°C) V. fischeri isolates grow faster. Therefore, V. logei symbionts are psychrophilic
compared to V. fischeri symbionts found in
Sepiola species. There are several Mediterranean
Sepiola species that live in the same coastal habitat, and
this provides an opportunity to test the present state and nature of
the symbiont population. Does the variety of Sepiola species
have an effect on the concentration and abundance of Vibrio symbionts in the sepiolid light organs, or do ecological factors (e.g.,
temperature) have a greater effect on the presence and dominance of
either symbiont in sepiolid light organs?
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MATERIALS AND METHODS |
Collection of specimens of Sepiola species and
isolation of Vibrio light organ symbionts.
Specimens
of sepiolid squids (Cephalopoda: Sepiolidae) (Table
1) (28) were collected from
depths of 20 to 75 m within 10 km of shore near the Laboratoire
Arago, Banyuls-sur-Mer, France. The water temperature and depth were
recorded at the time of collection in each case. The adult
Sepiola specimens were collected during May (S. affinis) and during July and September (S. affinis,
S. intermedia, S. ligulata, and S. robusta) (Table 2). The mantle lengths in adult specimens ranged from 10 to 30 mm. All specimens were
identified by using the criteria described by Bello (2). Squids were either flash frozen in liquid nitrogen to preserve the
bacteria in the light organs or kept alive until dissection and
isolation of the light organ symbionts. Once frozen, the bacterial light organ maintains the integrity of the bacteria and can be used
later for culturing bacteria in future analyses (12, 29, 33).
Once animals were collected, individual strains of
V. fischeri and
V. logei were isolated from adult
specimens of
S. affinis,
S. intermedia,
S. ligulata, and
S. robusta as previously described
(
5,
12) (Table
1). For live specimens, each squid was
anesthetized,
and the light organ was removed and subsequently
homogenized in
sterile seawater. Aliquots of the homogenate were spread
onto
seawater-tryptone-yeast extract (SWT) agar medium (
5),
and
duplicates were incubated at 18 and 26°C overnight. Frozen light
organs were also homogenized in this manner, and diluted homogenates
were spread onto SWT media to determine the concentrations of
individual
Vibrio species. Both
V. fischeri and
V. logei strains
were isolated from the preparations
incubated at 18 and 26°C,
and all strains used in the competition
experiments were isolated
at the same temperature so that the relative
growth abilities
of the strains were not biased. Once organisms were
isolated,
golden yellow colonies were observed on all plates, and
differences
in colony size were observed for some of the
isolates.
Chelex DNA isolation methods for the
Vibrio symbionts were
used to obtain templates for PCR amplification (
31).
Briefly,
DNA from an individual isolate was extracted by placing a
single
colony in 200 µl of 20 mM Trisbase-0.05 mM EDTA buffer (pH
7.4)
containing 5% (wt/vol) Chelex 100 resin (Bio-Rad Laboratories,
Richmond, Calif.). The cells were homogenized with an autoclaved
pestle
to prevent contamination, and the homogenate was incubated
at 80°C
for 25 min and then boiled for 10 min to denature proteins
and lyse the
cells. The cell debris and Chelex 100 were pelleted
by centrifugation,
and the supernatant fluid containing the DNA
was used as the bacterial
DNA template for PCR. The species identities
of individual
Vibrio colonies were confirmed by PCR amplification
of a
region of the 16S rDNA (designated region V1) that differentiates
V. fischeri from
V. logei (
12).
The PCR products were visualized
by ethidium bromide staining by using
a UV illuminator, and size
differences were determined by using the
amplified bands (
V. fischeri,
121 bp;
V. logei,
111 bp). Once identified, individual strains
were isolated and stored
for use in infection and competition
studies. The remaining colonies
were used for colony lifts for
identification of
V. fischeri and
V. logei strains.
Growth studies.
All of the bacterial strains used in this
study were inoculated into 5-ml starter cultures, which were then
transferred into flasks containing 50 ml of SWT broth so that the final
optical density at 600 nm was approximately 0.01 (5 × 107 cells/ml). The cultures were shaken at 225 rpm and were
grown at either 18 or 26°C. Optical density was measured periodically throughout the logarithmic growth phase. Each strain of V. fischeri or V. logei used in this study was isolated
from a Sepiola adult obtained from the Mediterranean Sea
(Table 1) and was identified by using the methods of Fidopiastis et al.
(12) and the methods described above.
Competition and infection experiments.
To determine whether
temperature has a direct effect on colonization potential and symbiont
composition, several symbiotic strains were analyzed to determine their
competitive abilities to infect light organs of juvenile
Sepiola squids (S. affinis and S. ligulata) by using a standard colonization method (19, 32). These isolates were used to test whether the species of host
determined the symbiotic composition or whether temperature was a
significant factor in establishing symbiotic competence. Newly hatched
S. affinis or S. ligulata juveniles were placed in vials containing 5 ml of seawater that was inoculated with 103 CFU of either one strain or, in competition
experiments, two strains of symbiotically competent bacteria. The
bacteria and squids were incubated at 18 and 26°C. After 12 h of
incubation, the juvenile squids were transferred to vials containing 5 ml of seawater without symbiotic bacteria. Since bacterial cells from
light organ homogenates have 100% plating efficiency (32), the actual extent of colonization could be calculated from the number
of CFU arising from aliquots of light organ homogenates that were
plated onto seawater nutrient agar medium (5, 6). After
48 h of incubation, juvenile squids were homogenized, and dilutions of the homogenates were plated onto seawater-tryptone agar to
determine the number of Vibrio cells resulting from either single-strain infections or two-strain competition infections (19). The relative abundance of each strain (inter- or
intraspecies) in a light organ was determined by either visual
luminescence of the CFU (30, 31) or by probing for the V1
variable region of the 16S rDNA (12) by using direct colony
lifts of the plated light organ homogenates (18). The V1
region probe was labeled by tailing oligonucleotide primers
(digoxigenin-dUTP; Boehringer Mannheim) and was hybridized to the
colony blots at 58°C overnight. The blots were washed under stringent
conditions (15 mM NaCl, 0.1 mM EDTA, 1% sodium dodecyl sulfate;
60°C), and colonies were detected with the fluorescent substrate
Vistra ECF (Amersham). All imaging in this study was performed with a
Molecular Dynamics model Storm 860 PhosphorImager. The percentages in
each competition experiment were calculated for each juvenile squid (30 squids/competition experiment), and the values were averaged and
arcsine transformed to test for significance (36).
Determination of symbiont composition in wild Sepiola
specimens.
Adult Sepiola specimens were collected at
various times throughout the year (Table 2), and the light organ
composition of each specimen was examined. All adult specimens were
identified by using morphological characteristics, as described by
Bello (2). The adult light organs and ink sac were dissected
out of the body cavity of each squid and frozen in liquid nitrogen until proper analysis could be completed at the home institution. After
freezing, each adult light organ was placed in sterile seawater or SWT
medium and homogenized. Serial dilutions were made in order to obtain a
reasonable number of CFU to plate onto SWT agar. The light organ
homogenates were incubated at both 18 and 26°C to determine whether
temperature had a pronounced effect on the relative abundance of each
Vibrio species. Individual CFU were isolated from the
homogenates, and colony lifts were used for analysis with the V1 region
16S rDNA probe in order to distinguish between V. fischeri
and V. logei from individual light organs (as in the competition assays). In addition to the V1 region 16S rDNA probe analysis, phenotypic typing of either V. fischeri or
V. logei strains was accomplished by using the protocol
described by Nishiguchi et al. (30).
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RESULTS |
Comparison of populations of V. fischeri and V. logei in adult sepiolids.
An analysis of the adult light
organ contents of four Sepiola species revealed that both
Vibrio species were present in all of the sepiolid species
examined (Table 2). The light organ populations of all S. affinis specimens were primarily composed of V. fischeri, independent of depth or temperature. The concentrations
of V. fischeri in S. affinis squids ranged from
98 to 99% of the total light organ isolates. The water temperatures at
the time of collection for all of the S. affinis adults
ranged from 18 to 22°C, and individuals were collected at depths of
20 m or less (Table 2). For all other species of squids (S. intermedia, S. ligulata, and S. robusta), the majority of the symbiotic bacteria found in the light organs were
V. logei (Table 2). The V. logei strains isolated
from these species of squids accounted for between 95 and 99% of the
total light organ contents during all collection periods (May to
September). These squid species were collected at depths ranging from
40 to 75 m, and the temperatures ranged from 10 to 16°C. During
the collecting season, the surface temperatures ranged from 24°C at the height of summer to 10°C in the winter months. Although summer sea surface temperatures are much higher than winter surface
temperatures, a distinct thermocline was formed between June and
September in all years that samples were obtained. At this time, the
water temperatures at depths below 25 m ranged from 12 to 16°C.
Growth of V. logei and V. fischeri in
vitro.
Table 1 shows all of the host squids and the bacterial
strains isolated and used in this study. Each strain of V. fischeri or V. logei was tested for growth at two
different temperatures (18 and 26°C) in SWT medium. Due to the
relative psychrophily of V. logei (12), the
growth constants were expected to be higher for V. logei at colder temperatures (<20°C) and higher for V. fischeri at warmer temperatures (>22°C). The growth constants for all strains of V. fischeri ranged from 0.4 to 0.6 h
1 at 18°C, whereas the growth constants were between
0.8 and 1.3 h1 for the same strains grown at 26°C
(Table 3). The V. logei
strains used in this study had optimal growth constants that ranged
from 0.9 to 1.4 h1 at 18°C and from 0.7 to 1.0 h1 at 26°C in culture. All strains were initially
isolated from different species of squid hosts on SWT agar at 18 and
26°C in order to avoid any bias which favored specific
temperature-acclimated strains.
Host specificity of Vibrio strains.
In addition to
the individual tests of bacterial strains in situ, I performed
experiments to determine whether strains isolated from one species of
squid were specific to their native host and if host specificity
provided a competitive advantage when the native squid species or a
nonnative species was infected. No differences in infection competency
were observed between S. affinis and S. ligulata
juveniles with V. fischeri native strains SA1, SA8, SL2, and
SL8 at either 26 or 18°C (Table
4). V. fischeri strains
isolated from S. intermedia or S. robusta squids
(designated SI and SR strains) did not exhibit any preference for
either of the two nonnative juvenile squid hosts at these temperatures
(Table 4). Similarly, no significant differences in specificity were
observed with S. affinis and S. ligulata
juveniles when they were infected with the native strains V. logei SA6, SA12, SL4, and SL12 at 26 or 18°C (Table
5). Again, V. logei strains
from S. intermedia and S. robusta (SI5, SI7, SR1,
and SR18) did not exhibit any specificity for juveniles of either of
the two squid species examined (Table 5).
In addition to strain specificity, all
V. fischeri and
V. logei strains were tested to determine their infectivity
at 18 and
26°C (Tables
4 and
5) at the end of a 48-h incubation
period.
All of the
V. fischeri strains inoculated and
incubated at 26°C
infected both
S. affinis and
S. ligulata juveniles at concentrations
at least 10-fold higher than
the concentrations of the strains
inoculated and incubated at 18°C
(Table
4). No significant differences
were observed with the
V. fischeri strains examined at the same
temperature (Table
4).
Conversely,
V. logei strains inoculated
and incubated at
26°C were present at concentrations that were
approximately 10-fold
lower than the concentrations of the strains
tested at 18°C (Table
5). Again, no differences were observed
with
V. logei
strains tested at the same temperature (18 or 26°C)
(Table
5).
V. fischeri strains from
S. intermedia and
S. robusta were also tested at different temperatures with
nonnative host
squid species (Table
4), and no difference was observed
between
these strains and the native strains tested at the
same temperature
(either 18 or 26°C). Similarly, no differences
were observed for
V. logei strains isolated from
S. intermedia or
S. robusta when
they were
measured at the temperatures used for strains obtained
from
S. affinis or
S. ligulata (Table
5).
Competition within and between V. fischeri and V. logei strains in Sepiola juveniles.
Since no
intraspecies differences in growth and infection were observed for
the V. fischeri or V. logei strains tested,
only one representative strain was used for the following competition experiments. V. fischeri native strain SA1 isolated from
S. affinis was used in competition experiments with all of
the other V. fischeri strains (SL8, SI2, SR5) at 26°C, and
no discernable preference was observed among the V. fischeri
strains examined (Table 6). Similarly,
V. fischeri native strain SL8 from S. ligulata was not preferred over other nonnative strains when it
was used in competition experiments performed with S. ligulata juveniles (Table 6). V. logei native
strains SA6 and SL12 isolated from S. affinis and
S. ligulata, respectively, were also tested at 18°C
and exhibited no preference for either squid species during competition
with all other V. logei strains used in this study (Table
7). None of the SI and SR strains
exhibited specificity for either S. affinis or S. ligulata juveniles when competition experiments were performed at
26 or 18°C.
In competition experiments performed at 26°C, all juveniles,
regardless of species, were infected primarily with
V. fischeri strains regardless of the species from which they were
isolated
(Table
8). The majority of
V. fischeri colonies were much larger
than the
V. logei colonies arising from the homogenized juvenile
light organs.
The
V. fischeri in both
S. affinis and
S. ligulata juvenile light organs accounted for 78 to 95% of the
total light
organ population in squids incubated at 26°C (Table
8).
Conversely,
all light organ competition experiments performed at 18°C
resulted
in colonization primarily by
V. logei isolates from
all four squid
species sampled (Table
8). In these competition
experiments,
V. logei symbionts accounted for 77 to 96% of
the total light
organ population (Table
8). The colonies were primarily
the same
size, and only colony blots or visibly luminous colony
morphology
(
30) could indicate the difference between
V. logei and
V. fischeri symbionts.
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TABLE 8.
Effect of temperature on the ratio of V. fischeri cells to V. logei cells present in juvenile
Sepiola light organs after 48 h
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DISCUSSION |
Previous studies of luminous bacterium-squid symbioses showed that
host light organs were monotypic (22). Until recently, no
other species of luminous bacteria were known to exist in members of
the Sepiolidae. Recently, Fidopiastis et al. (12) reported that a second Vibrio species is present only in
Mediterranean species of sepiolids. This finding suggests that luminous
bacterium-squid mutualisms are not species specific but may depend on
environmental factors. In this study I investigated the abiotic factors
that affect this two-symbiont association and whether temperature
influences the degree to which different symbiotic vibrios infect
sepiolid squid hosts.
Sepiolid light organ pores are continually open to the surrounding
seawater, which potentially provides access for any type of bacterium
in the squid habitat. The presence of only V. fischeri or
V. logei in the Sepiola light organ shows that
there are strong species-specific interactions between these bacteria
and their hosts. In the related genus Euprymna, the numbers
of bacterial cells are controlled in part by diel venting of
approximately 90% of bacteria through the lateral pores of the light
organ into the mantle cavity (5, 6). This venting behavior
results in a sufficiently high density of symbiotically competent
Vibrio cells in the water column to promote colonization of
the next generation of juvenile squids (19). Thus,
symbiotically competent bacteria that are present in the
environment can influence the composition of the squid light organ,
particularly if more than one species is present. Strict species
recognition does not occur for V. fischeri or V. logei in Mediterranean Sepiola squids, and it appears
that one of the more influential factors determining light organ
composition is the temperature at which the host is infected and
persists. In previous studies to investigate the influence of
temperature acclimation in Escherichia coli (3, 24), workers have shown that the genetics of a particular strain has no discernable effect on adaptation to a different environment but
does influence the fitness of the strain (4). One may
conclude that the sepiolid symbiosis is species specific (V. fischeri and/or V. logei), but the variability in light
organ composition and the ability of both symbiont species to infect
different host squids at different temperatures indicate how
environmental factors can influence the distribution and population
dynamics of symbiont colonization.
The degree of relatedness and diversity among numerous symbiotic taxa
has traditionally been thought of as a good predictor of cospeciation
(17). However, recently, a number of examples have
demonstrated that the systematics underlying symbiosis is not as clear
as we have traditionally thought (1, 10, 11, 15, 16, 25,
31). Changes in the host association with a particular symbiont
may be related to selection pressure on the host's fitness and how the
symbiont may or may not affect future generations of host-symbiont
pairs (13, 35). Population size and the availability of
hosts that can be infected also affect the pairing of host-symbiont
associations and possibly the specificity that a mutualism eventually
expresses (7, 37). The presence of two species of symbionts
that can both infect different host species may be an initial step in
establishing a monotypic host-symbiont association. However, how the
natural balance between host fitness and symbiont competence is
established remains to be determined (14). Because there are
several sympatric Sepiola host species living in the area
sampled, the possibility of host switching between squids and the
establishment of host-symbiont specificity can be studied. In future
experiments researchers should examine the degree to which ecological
and/or genetic factors control patterns of cospeciation and evolution
and how we can better predict which patterns arise from these factors.
Whether the symbionts determine new avenues for host evolution and
radiation into different ecological habitats in this family of squids
is just one of the many questions that should be pursued in future studies.
| |
ACKNOWLEDGMENTS |
I thank S. von Boletzky for help with collecting
Sepiola adults and egg masses at Laboratoire Arago,
Banyuls-sur-mer, France, and for providing insight and knowledge of the
Mediterranean Sepiolidae. I also thank J. L. Botsford, D. J. Howard, and J. Randall for reviewing the manuscript prior to submission
and M. J. McFall-Ngai and E. G. Ruby of the University of
Hawaii for providing insight and supporting my work on the
sepiolid-Vibrio symbiosis. I thank C. L. Lickliter of
my laboratory at New Mexico State University for providing bacterial
growth data.
This work was supported by a summer research grant from the Arts and
Sciences research center at New Mexico State University and by the
University Research Expeditions Program (UREP), University of California.
| |
FOOTNOTES |
*
Mailing address: Department of Biology, New Mexico
State University, Box 30001, MSC 3AF, Las Cruces, NM 88003-8001. Phone: (505) 646-3721. Fax: (505) 646-5665. E-mail: nish{at}nmsu.edu.
| |
REFERENCES |
| 1.
|
Baumann, P.,
N. A. Moran, and L. Baumann.
1997.
The evolution and genetics of aphid endosymbionts.
BioScience
47:12-20.
|
| 2.
|
Bello, G.
1995.
A key for identification of the Mediterranean sepiolids (Mollusca: Cephalopoda).
Bull. Inst. Oceanogr. (Monaco)
16:41-55.
|
| 3.
|
Bennett, A. F., and R. E. Lenski.
1993.
Evolutionary adaptation to temperature. II. Thermal niches of experimental lines of Escherichia coli.
Evolution
47:1-12.
|
| 4.
|
Bennett, A. F., and R. E. Lenski.
1998.
Evolutionary adaptation to temperature. VI. Phenotypic acclimation and its evolution in Escherichia coli.
Evolution
51:36-44.
|
| 5.
|
Boettcher, K. J., and E. G. Ruby.
1990.
Depressed light emission by symbiotic Vibrio fischeri of the sepiolid squid Euprymna scolopes.
J. Bacteriol.
172:3701-3706[Abstract/Free Full Text].
|
| 6.
|
Boettcher, K. J.,
E. G. Ruby, and M. J. McFall-Ngai.
1996.
Bioluminescence in the symbiotic squid Euprymna scolopes is controlled by a daily biological rhythm.
J. Comp. Physiol.
179:65-73.
|
| 7.
|
Bull, J. J.,
I. J. Molineux, and W. R. Rice.
1991.
Selection of benevolence in a host-parasite system.
Evolution
45:875-882[CrossRef].
|
| 8.
|
Cary, S. C.
1994.
Vertical transmission of a chemoautotrophic symbiont in the photobranch bivalve, Solemya reidi.
Mol. Biol. Biotechnol.
3:121-130.
|
| 9.
|
Cavanaugh, C. M.
1994.
Microbial symbiosis: patterns of diversity in the marine environment.
Am. Zool.
34:79-89.
|
| 10.
|
Distel, D. L.,
H. Felbeck, and C. M. Cavanaugh.
1994.
Evidence for phylogenetic congruence among sulfur-oxidizing chemoautotrophic bacterial endosymbionts and their bivalve hosts.
J. Mol. Evol.
38:533-542[CrossRef].
|
| 11.
|
Distel, D. L.
1998.
Evolution of chemoautotrophic endosymbioses in bivalves.
BioScience
48:277-286[CrossRef].
|
| 12.
|
Fidopiastis, P. M.,
S. von Boletzky, and E. G. Ruby.
1998.
A new niche for Vibrio logei, the predominant light organ symbiont of squids in the genus Sepiola.
J. Bacteriol.
180:59-64[Abstract/Free Full Text].
|
| 13.
|
Frank, S. A.
1996.
Host-symbiont conflict over the mixing of symbiotic lineages.
Proc. R. Soc. London Biol. Sci.
263:339-344[Medline].
|
| 14.
|
Frank, S. A.
1996.
Host control of symbiont transmission: the separation of symbionts into germ and soma.
Am. Nat.
148:1113-1124[CrossRef].
|
| 15.
|
Haygood, M. G., and D. L. Distel.
1993.
Bioluminescent symbionts of flashlight fishes and deep-sea anglerfishes from unique lineages related to the genus Vibrio.
Nature
363:154-156[CrossRef][Medline].
|
| 16.
|
Hinkle, G.,
J. K. Wetterer,
T. R. Schultz, and M. L. Sogin.
1994.
Phylogeny of the attine ant fungi based on analysis of small subunit rRNA gene sequences.
Science
266:1695-1697[Abstract/Free Full Text].
|
| 17.
|
Law, R.
1985.
Evolution in a mutualistic environment, p. 145-170.
In
D. H. Boucher (ed.), The biology of mutualism: ecology and evolution. Oxford University Press, New York, N.Y.
|
| 18.
|
Lee, K.-H., and E. G. Ruby.
1992.
Detection of the light organ symbiont, Vibrio fischeri, in Hawaiian seawater by using lux gene probes.
Appl. Environ. Microbiol.
58:942-947[Abstract/Free Full Text].
|
| 19.
|
Lee, K.-H., and E. G. Ruby.
1994.
Effect of the squid host on the abundance and distribution of symbiotic Vibrio fischeri in nature.
Appl. Environ. Microbiol.
60:1565-1571[Abstract/Free Full Text].
|
| 20.
|
Lee, K.-H., and E. G. Ruby.
1994.
Competition between Vibrio fischeri strains during the initiation and maintenance of a light organ symbiosis.
J. Bacteriol.
176:1985-1991[Abstract/Free Full Text].
|
| 21.
|
Mangold, K., and S. von Boletzky.
1988.
Mediterranean cephalopod fauna, p. 315-330.
In
M. R. Clarke, and E. R. Trueman (ed.), The Mollusca, vol. 12. Academic Press, San Diego, Calif.
|
| 22.
|
McFall-Ngai, M. J., and E. G. Ruby.
1991.
Symbiont recognition and subsequent morphogenesis as early events in an animal-bacterial mutualism.
Science
254:1491-1494[Abstract/Free Full Text].
|
| 23.
|
McFall-Ngai, M. J., and E. G. Ruby.
1998.
Sepiolids and vibrios: when they first meet.
BioScience
48:257-265[CrossRef].
|
| 24.
|
Mongold, J. A.,
A. F. Bennett, and R. E. Lenski.
1996.
Evolutionary adaptation to temperature. IV. Adaptation of Escherichia coli at a niche boundary.
Evolution
50:35-43[CrossRef].
|
| 25.
|
Moran, N. A., and A. Telang.
1998.
Bacteriocyte-associated symbionts of insects.
BioScience
48:295-304[CrossRef].
|
| 26.
|
Munson, M. A.,
P. Baumann,
M. A. Clark,
L. Baumann,
N. A. Moran, and D. J. Voegtlin.
1991.
Evidence for the establishment of aphid-eubacterial endosymbiosis in an ancestor of four aphid families.
J. Bacteriol.
173:6321-6324[Abstract/Free Full Text].
|
| 27.
|
Nealson, K. H., and J. W. Hastings.
1991.
The luminous bacteria, p. 625-639.
In
A. Balows, H. G. Truper, M. Dworkin, W. Harder, and K. H. Schleifer (ed.), The prokaryotes. A handbook on the biology of bacteria: ecophysiology, isolation, identification, applications, 2nd ed. Springer-Verlag, New York, N.Y.
|
| 28.
|
Nesis, K. N.
1987.
Cephalopods of the world.
T.F.H. Publications, Neptune City, N.J.
|
| 29.
|
Nishiguchi, M. K.,
L. H. Lamarcq,
E. G. Ruby, and M. J. McFall-Ngai.
1996.
Competitive dominance of native strain symbiotic bacteria measured by colonization and in situ hybridization.
Am. Zool.
36:41A.
|
| 30.
|
Nishiguchi, M. K.,
E. G. Ruby, and M. J. McFall-Ngai.
1997.
Phenotypic bioluminescence as an indicator of competitive dominance in the Euprymna-Vibrio symbiosis, p. 123-126.
In
J. W. Hastings, J. W. Kricka, and P. E. Stanley (ed.), Bioluminescence and chemiluminescence: molecular reporting with photons. J. Wiley and Sons, New York, N.Y.
|
| 31.
|
Nishiguchi, M. K.,
E. G. Ruby, and M. J. McFall-Ngai.
1998.
Competitive dominance among strains of luminous bacteria provides an unusual form of evidence for parallel evolution in sepiolid squid-Vibrio symbioses.
Appl. Environ. Microbiol.
64:3209-3213[Abstract/Free Full Text].
|
| 32.
|
Ruby, E. G., and L. M. Asato.
1993.
Growth and flagellation of Vibrio fischeri during initiation of the sepiolid squid light organ symbiosis.
Arch. Microbiol.
159:160-167[CrossRef][Medline].
|
| 33.
|
Ruby, E. G.
1996.
Lessons from a cooperative, bacterial-animal association: the Vibrio fischeri-Euprymna scolopes light organ symbiosis.
Annu. Rev. Microbiol.
50:591-624[CrossRef][Medline].
|
| 34.
|
Saffo, M. B.
1992.
Invertebrates in endosymbiotic associations.
Am. Zool.
32:557-565.
|
| 35.
|
Sniegowski, P. D.,
P. J. Gerish, and R. E. Lenski.
1997.
Evolution of high mutation rates in experimental populations of Escherichia coli.
Nature
387:703-705[CrossRef][Medline].
|
| 36.
|
Sokal, R. R., and F. J. Rohlf.
1981.
Biometry. W. H.
Freeman and Co., New York, N.Y.
|
| 37.
|
Turner, P. E.,
F. S. Cooper, and R. E. Lenski.
1998.
Tradeoff between horizontal and vertical modes of transmission in bacterial plasmids.
Evolution
52:315-329[CrossRef].
|
Applied and Environmental Microbiology, August 2000, p. 3550-3555, Vol. 66, No. 8
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Copyright © 2000, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
