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Applied and Environmental Microbiology, September 1998, p. 3209-3213, Vol. 64, No. 9
Pacific Biomedical Research Center,
University of Hawai'i, Manoa, Honolulu, Hawaii 96813
Received 20 April 1998/Accepted 22 June 1998
One of the principal assumptions in symbiosis research is that
associated partners have evolved in parallel. We report here experimental evidence for parallel speciation patterns among several partners of the sepiolid squid-luminous bacterial symbioses. Molecular phylogenies for 14 species of host squids were derived from sequences of both the nuclear internal transcribed spacer region and the mitochondrial cytochrome oxidase subunit I; the glyceraldehyde phosphate dehydrogenase locus was sequenced for phylogenetic
determinations of 7 strains of bacterial symbionts. Comparisons of
trees constructed for each of the three loci revealed a parallel
phylogeny between the sepiolids and their respective symbionts. Because
both the squids and their bacterial partners can be easily cultured
independently in the laboratory, we were able to couple these
phylogenetic analyses with experiments to examine the ability of the
different symbiont strains to compete with each other during the
colonization of one of the host species. Our results not only indicate
a pronounced dominance of native symbiont strains over nonnative
strains, but also reveal a hierarchy of symbiont competency that
reflects the phylogenetic relationships of the partners. For the first
time, molecular systematics has been coupled with experimental
colonization assays to provide evidence for the existence of parallel
speciation among a set of animal-bacterial associations.
Cooperative associations with
symbiotic bacteria are a common and ancient theme in the biology of
animal and plant life. Thus, it is not surprising that there is often
congruency between the evolutionary patterns of closely related host
species and their symbiotic partners (1, 6, 11, 13). This
congruency, known as parallel cladogenesis, has been revealed by
comparing the sequences of genes that have rates of divergence suitable for such studies. However, because most animal-bacterial associations cannot be experimentally initiated, the mechanisms underlying the
processes of cospeciation and host-symbiont specificity have not been
explored.
The luminescent organ associations between sepiolid squids and luminous
bacteria provide an unusually tractable system for the study of the
evolution of symbiosis because (i) both the host and symbiont can be
cultured and maintained in the laboratory (10, 19); (ii)
newly hatched squids are colonized by symbiotic bacteria from the
environment, allowing the association to be initiated and monitored
experimentally (for review, see reference 26); and
(iii) the numerous sepiolid squid species have a wide biogeographic
distribution (22). The ease of studying both the squid host
and its bacterial symbiont separately or combined under experimental
conditions allows one to examine whether a particular squid host can
distinguish its own natural symbiont from those of other sepiolid squid
species (17) and whether this specificity reflects the
evolution of the partnership. While coevolution has been experimentally
studied in certain plant-bacterial systems (31, 33), the
squid-vibrio symbiosis offers a unique opportunity to do so among
animal-bacterial associations.
In the present study, the sequences of one nuclear locus and one
mitochondrial locus have been used to generate phylogenetic trees for
several species of sepiolids from Indo-West Pacific, Eastern Pacific,
Mediterranean, and Atlantic populations. For a subset of the species,
we determined the phylogenetic relationships of their symbiotic
bacteria. An analysis of these data showed congruency between the
derived phylogenetic trees of the hosts and their symbionts. In
experiments in which two symbiotic bacterial strains were both present
during the colonization of a representative host species, a hierarchy
of competitive dominance was derived that mirrored the congruency
pattern of these phylogenetic trees. Taken together, these data suggest
that cospeciation has occurred during the evolution of the squid-vibrio
symbioses and that initial recognition processes are key specificity
determinants in these associations. These results provide the first
experimentally derived support of cospeciation between animal hosts and
their bacterial symbionts.
Generation of molecular phylogenies.
Squid specimens and
their bacterial symbionts were collected alive at nine different
geographic locations (Table 1). In
addition, formalin- or ethanol-preserved specimens of Euprymna
stenodactyla, Sepiola atlantica, Sepiola
aurantica, Sepiola ligulata, Sepiola rondoletti, Rossia macrosoma, and Heteroteuthis
dispar were obtained from various museum and private collections.
Bacterial symbionts were identified as either Vibrio
fischeri, Vibrio logei, or Photobacterium leiognathi as previously described (7, 25). Only light
organ isolates of sepiolid species that were identified as V. fischeri were compared in this study (7).
0099-2240/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Competitive Dominance among Strains of Luminous Bacteria Provides
an Unusual Form of Evidence for Parallel Evolution in Sepiolid
Squid-Vibrio Symbioses
ABSTRACT
Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
INTRODUCTION
Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
TABLE 1.
Geographical collection sites and symbiont
characteristics for specimens of squids from the families Sepiolidae
and Loliginidae
-mercaptoethanol, 0.1% (wt/vol)
polyvinylpyrrolidone, and 0.1% (wt/vol) sodium dodecyl sulfate (SDS).
The homogenate was incubated at 60°C for 60 min, an equal volume of a
chloroform-isoamyl alcohol mixture (24:1) was then added, and the
suspension was centrifuged at 10,000 × g for 10 min. A
two-thirds volume of cold isopropanol was added to the resulting
aqueous phase, and this solution was placed at 
20°C overnight to
precipitate the DNA. The DNA was then pelleted, resuspended in 2.5 ml
of TE buffer (10 mM Tris-HCl and 1 mM EDTA [pH 8.0]) containing
2.6 g of CsCl2, and centrifuged at 270,000 × g for 8 h at 20°C. The isolated genomic DNA fraction
was then reprecipitated with 95% ethanol, washed with 70% ethanol,
dried, and resuspended in TE buffer.
To isolate DNA from fixed animal tissues, between 1 and 10 mg of tissue
was extracted at 65°C in 500 µl of a buffer containing 1 mM NaCl, 1 mM Tris-HCl, 0.1 mM EDTA (pH 7.5), and 0.2% (vol/vol) SDS, to which
was added 250 µl of 7 M ammonium acetate (12). The
homogenate was centrifuged, and the DNA was precipitated, washed, and
resuspended in TE buffer as described above.
DNA templates for sequence analyses were obtained by PCR amplification.
Each 100-µl PCR mixture contained 1 µl of template DNA solution,
0.01 µM (each) PCR primer, and 200 µM total deoxynucleoside triphosphates. DNA from sepiolid species was amplified with PCR primers
specific for either their internal transcribed spacer (ITS) region
between the 18S and 25S rRNA genes (1,425 to 1,450 bp in length,
including ITS region 1, the 5.8S gene, and ITS region 2) or their
cytochrome oxidase subunit I (COI) sequence (700 bp in length). For the
ITS region, the PCR primer sequences were those reported by Goff et al.
(9). The amplification conditions used were 25 cycles of
94°C for 75 s, 55°C for 2 min, and 72°C for 4 min. The ITS
regions for several species could not be amplified because of the poor
condition of the template DNA, particularly from formalin-fixed
specimens. Because the ITS exists in several genomic copies, two or
three different ITS fragments from an individual of each species were
cloned and sequenced to estimate the extent of both interclonal and
within-individual variation. For the COI region, universal primers
(8) were used under the following amplification conditions:
25 cycles of 94°C for 50 s, 50°C for 75 s, and 72°C for
90 s. PCR fragments were directly sequenced in both directions by
using an automated sequencer. Sequencing of the entire ITS region
required an additional two internal primers: 5'-TCGTCGATCGGAGACGCGGC-3'
(forward) and 5'-CCTCCACAGTGTTTCTTCAC-3' (reverse).
DNA was isolated from strains of symbiotic bacteria (Table 1) that were
cultured from the luminescent organs of freshly collected squid hosts
as previously described (3). The bacterial DNA recovered
from the luminescent organs of fixed host specimens was not suitable
for sequencing. To extract DNA, individual colonies were homogenized in
200 µl of a buffer composed of 20 mM Tris-HCl and 0.05 mM EDTA (pH
7.4), and containing 5% (wt/vol) Chelex-100 resin (Bio-Rad
Laboratories, Richmond, Calif.). 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 was pelleted by centrifugation, and the
supernatant fluid was used as the bacterial DNA template for PCR. DNA
was amplified with primers specific for the glyceraldehyde phosphate
dehydrogenase (gapA) gene (15) as previously
described (16). To derive phylogenetic trees for both the
hosts and the symbionts, DNA sequences were analyzed by parsimony
analysis with PAUP 3.1.1 (3), and the maximum likelihood
calculations were made with PHYLIP, version 3.5 (24), and
fastDNAml (24), with no assumption of a molecular clock.
Colonization experiments. For determinations of either the extent of colonization or the degree of competitiveness between different strains of symbiotic bacteria, we used the standard colonization assay as previously described (17, 27). Briefly, newly hatched Euprymna scolopes squid were placed in vials containing 5 ml of seawater, to which approximately 104 CFU of either one or, for competition experiments, two strains of symbiotically competent bacteria had been added. After 12 h of incubation, the juvenile squid were transferred to vials containing 5 ml of seawater without symbiotic bacteria. The progress of light organ colonization was periodically monitored by measuring the luminescence of each squid with a sensitive photometer (model 3000; Biospherical Instruments, San Diego, Calif.). Because bacterial cells from light organ homogenates have essentially a 100% plating efficiency (27), the actual extent of colonization could be calculated from the number of CFU arising from aliquots of light organ homogenates that were plated on seawater nutrient agar medium (3). Different clutches of E. scolopes eggs were used in at least three replicate competition experiments to ensure that the results were not affected by any interclutch variation in colonization characteristics. Forty-eight hours after inoculation, the relative degree of colonization by the two competing bacterial strains from different host species was quantified by plating homogenates of light organs of E. scolopes juveniles exposed to mixtures of the strains (17). As previously described (23), the relative abundance of each strain in the light organ was determined by the visually distinct and genetically stable differences in the luminescence intensities of colonies of these different strains.
Nucleotide sequence accession number. The sequences reported in this paper have been deposited in the GenBank database under the following accession numbers: ITS sequences, AF031881 to AF031885, AF034558 to AF034565, and AF034844; COI sequences, AF035701 to AF035715 and AF036912; and gapA sequences, AF034845 to AF034851.
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RESULTS |
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Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
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Molecular phylogenies. The ITS and COI sequences of squid specimens were compared for within-species variation and between-species divergence. No differences were found in the >1,400-bp ITS locus between separate clones derived from an individual animal, and less than 0.1% sequence variation occurred between any two or three individuals of the same squid species at the ITS locus. Sequence divergence rates ranged from 2% (between species) to 12% (between species in the same genus and outgroups). Similarly, there was no variation observed between individuals of the same species at the COI locus, and the sequence divergence rates ranged from 3.5% to 22%.
The branching patterns of phylogenetic trees derived from sequences of each of these two loci, by either the parsimony or maximum-likelihood method of analysis, were similar. However, while in all cases Euprymna species clustered together, as did species of Sepiola (Fig. 1), the ITS and COI data sets revealed some minor differences in the species relationships within these clades. Specifically, the relative position of Euprymna morsei varied slightly between the trees. In addition, whereas the ITS data resolved the relationship between the species Sepiola affinis, Sepiola intermedia, and Sepiola robusta, the COI data did not. In both trees, species of the Pacific genera, Euprymna, which bear light organs, and Rossia, which do not, clustered more closely together than Euprymna and Sepiola, which both bear light organs. Similarly, species of the Mediterranean genera, Sepiola, which bear light organs, and Sepietta, which do not, clustered more closely together. The ITS locus of Heteroteuthis dispar, a mesopelagic squid from the Atlantic, could not be completely recovered for sequencing. However, the analyses of COI sequences of this species supported it as an outgroup to all species examined other than Loliolus noctiluca, a loliginid squid with a bacterial light organ, that formed the family-level outgroup for both the ITS and COI loci.
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Competitive dominance. When presented individually, all bacterial strains isolated from Euprymna species were capable of initiating and maintaining a typical level of symbiotic colonization of juvenile E. scolopes; i.e., at 24 and 48 h postinoculation, there were between 3 × 105 and 10 × 105 CFU per light organ (data not shown and reference 28). In contrast, SA1, the Sepiola light organ symbiont strain, while able to colonize E. scolopes juveniles, was less effective, reaching a population level of no more than 3 × 105 CFU per light organ. Strain LN101, the light organ symbiont of L. noctiluca, belongs to the distinct luminous species P. leiognathi (Table 1) and has no ability to colonize the E. scolopes light organ.
In all of the competition experiments using symbionts from sepiolid squids, it was observed that 12 h following inoculation, the two strains were present in the light organ at approximately a 1:1 ratio, indicating that these strains were equally competent in initiating a symbiotic colonization (data not shown). However, after 48 h, the native strain, ES114, had achieved a greater than 20-fold advantage over any of the nonnative strains tested (Table 3). When strains from the other two Euprymna species were presented to juveniles of E. scolopes, the strain from E. morsei (EM17), exhibited a fourfold competitive dominance over the Euprymna tasmanica strain (ET101); however, the E. tasmanica strain outcompeted the symbiont from S. affinis (SA1). Thus, the hierarchy among symbiont strains isolated from sepiolid species mirrors the relatedness between the squid-symbiont pairs as derived from the molecular phylogenetic analyses (Fig. 1).
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DISCUSSION |
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Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
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In this paper, we present (i) the derived molecular phylogenies of an array of sepiolid squids and their symbiont strains, (ii) an analysis of these phylogenies that revealed parallel cladogenesis between these partners, and (iii) an experimental demonstration that a hierarchy exists in the ability of bacterial symbionts from different species of squids to colonize the Hawaiian squid, E. scolopes.
The systematic relationships among the Sepiolidae have not been adequately revealed by morphological data alone (2), and the fossil record of this group is limited. Thus, molecular data present a particularly valuable approach to resolving the relationships within this family. The phylogenies derived from ITS and COI sequences separated the Sepiola species and the Euprymna species into monophyletic genera (Fig. 1). In addition, the arrangement of squid species on these trees suggests either that luminescent organs arose independently in the evolution of these two genera or that they were lost within members of the genera Sepietta and Rossia.
Although the ITS and COI data resolved the Sepiola species and Euprymna species into two independent groupings, some variability existed between the branching patterns at the species level. Specifically, in the phylogeny derived by using the COI data, E. morsei was more closely related to E. tasmanica and E. stenodactyla than it was to E. scolopes, whereas the ITS data suggested that E. morsei is the sister taxon to E. scolopes (Fig. 1). In addition, the COI tree did not resolve the relationship of the Sepiola species; however, although the COI locus was less useful in certain aspects of these analyses, consideration of the ITS and the COI loci together provided a stronger basis of support for possible coordinate processes occurring in the evolution of these symbioses. The value of data derived from nuclear (ITS), relative to mitochondrial (COI), gene sequences in revealing phylogenies is a controversial issue (14, 20, 21). Thus, analyses based on these two separate gene trees still leave the species tree unresolved. Even with additional molecular phylogenetic data and more knowledge of the life histories of the animals, this issue may not be resolved. However, other results in this paper may be viewed as providing additional support for the ITS tree, i.e., the gapA phylogeny for the bacterial symbionts (Fig. 1B) and the competitive hierarchy from the colonization experiments (Table 3).
The phylogenies derived from the analyses of the squid ITS and the symbiont gapA loci support congruent evolution of host-symbiont pairs. Similar studies with other symbiotic relationships using molecular and/or morphological data have provided evidence that many associations (e.g., chemoautotrophic symbioses, ant-fungal mutualisms, and aphid-Buchnera relationships) are phylogenetically congruent (1, 4, 5, 13). While molecular phylogenetic analysis has been a powerful method to approach these questions, under some circumstances, it has not been able to resolve patterns of parallel cladogenesis (11). Such problems with phylogenetic analyses would benefit from independent measures of congruent evolution.
The ability to manipulate experimentally the sepiolid-bacterial associations offers a series of methods that provide a powerful complementation to phylogenetic analyses. In the present study, we tested whether parallel cladogenesis was reflected in the dynamics of the initiation of this symbiosis. The hierarchy that was observed among the symbionts of the seven squid species tested directly reflected the relative ITS-gapA phylogenies derived for the host animals and their specific symbionts and provided additional support for the evolution of strain specificity and partner fidelity in squid light organ associations. The hierarchical patterns that we observed in the colonization experiments may also provide insight into the processes that occur during divergence of coevolving species. The data showed two patterns: (i) Euprymna symbionts were capable of infecting E. scolopes juveniles fully, but demonstrated a competitive dominance hierarchy; and (ii) Sepiola symbionts were less competitive than the Euprymna strains. These data suggest either that the Euprymna and the Sepiola associations evolved independently or that their divergence included a two-step process, i.e., a change in symbiotic characters that influenced competitiveness, followed by a loss of traits that allowed full colonization.
Because these symbioses can be experimentally initiated, study of the sepiolid associations promises to advance our understanding of host-symbiont evolution. Future studies will pursue two directions: (i) to continue to use the variety of sepiolid species and their symbionts to study parallel evolutionary relationships and (ii) to study the mechanisms that drive the molecular basis for specificity and speciation. For example, examination of the several sympatric species of Sepiola in the Mediterranean (18) will reveal whether each of these squid species is coevolving with a specific lineage of symbionts, or whether instead they all share a common pool of symbionts. In addition, the discovery that symbionts from divergent Euprymna species express different degrees of colonization dominance provides a model for identifying the biochemistry underlying the evolution of specificity and recognition in a host-bacterial interaction. Finally, as has been the case in the plant root nodule symbioses, molecular genetic manipulation of bacterial light organ symbionts has begun to reveal the genes involved in symbiotic competency (26, 32) and should lead ultimately to an understanding of the biochemical mechanisms underlying species specificity in this cooperative partnership.
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ACKNOWLEDGMENTS |
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We thank P. Baumann, N. Davies, G. Roderick, and members of the M.M.N. and E.G.R. laboratories for their comments and suggestions. Squid specimens were caught or donated by S. von Boletzky, A. Guerra, F. G. Hochberg, M. Norman, T. Okutani, R. Villanueva, and R. Young. The ITS external primers were obtained from L. Goff. Automated sequencing was performed with the assistance of G. Bernardi. PAUP analysis was performed under the auspices of D. Eernisse.
This research was supported by National Science Foundation grants OCE-9321645 (Marine Biotechnology Fellowship) to M.K.N. and IBN-96-01155 (to M.M.N. and E.G.R.), as well as by Office of Naval Research awards N00014-91-J-1357 and N00014-93-I-0846 to M.M.N. and E.G.R., respectively, and NIH R01 RR10926 (to E.G.R. and M.M.N.).
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FOOTNOTES |
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* Corresponding author. Mailing address: Pacific Biomedical Research Center, University of Hawai'i, Manoa, 41 Ahui St., Honolulu, HI 96813. Phone: (808) 539-7310. Fax: (808) 599-4817. E-mail: mcfallng{at}hawaii.edu.
Present address: Department of Biology, New Mexico State
University, Las Cruces, NM 88003-8001.
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Top
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Materials & Methods
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Discussion
References
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Applied and Environmental Microbiology, September 1998, p. 3209-3213, Vol. 64, No. 9
0099-2240/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
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