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Applied and Environmental Microbiology, November 2000, p. 4916-4920, Vol. 66, No. 11
0099-2240/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Viral Impacts on Total Abundance and Clonal
Composition of the Harmful Bloom-Forming Phytoplankton
Heterosigma akashiwo
Kenji
Tarutani,
Keizo
Nagasaki,* and
Mineo
Yamaguchi
Harmful Phytoplankton Section, Harmful Algal
Bloom Division, National Research Institute of Fisheries and
Environment of Inland Sea, 2-17-5 Maruishi, Ohno, Saeki, Hiroshima
739-0452, Japan
Received 21 April 2000/Accepted 29 August 2000
 |
ABSTRACT |
Recent observations that viruses are very abundant and biologically
active components in marine ecosystems suggest that they probably
influence various biogeochemical and ecological processes. In this
study, the population dynamics of the harmful bloom-forming phytoplankton Heterosigma akashiwo (Raphidophyceae) and the
infectious H. akashiwo viruses (HaV) were monitored in
Hiroshima Bay, Japan, from May to July 1998. Concurrently, a number of
H. akashiwo and HaV clones were isolated, and their virus
susceptibilities and host ranges were determined through laboratory
cross-reactivity tests. A sudden decrease in cell density of
H. akashiwo was accompanied by a drastic increase
in the abundance of HaV, suggesting that viruses contributed
greatly to the disintegration of the H. akashiwo bloom as mortality agents. Despite the large
quantity of infectious HaV, however, a significant proportion of
H. akashiwo cells survived after the bloom
disintegration. The viral susceptibility of H. akashiwo isolates demonstrated that the majority of these
surviving cells were resistant to most of the HaV clones, whereas
resistant cells were a minor component during the bloom period.
Moreover, these resistant cells were displaced by susceptible cells,
presumably due to viral infection. These results demonstrated that
the properties of dominant cells within the H. akashiwo population change during the period when a bloom is
terminated by viral infection, suggesting that viruses also play an
important role in determining the clonal composition and maintaining
the clonal diversity of H. akashiwo populations.
Therefore, our data indicate that viral infection influences the
total abundance and the clonal composition of one host algal species,
suggesting that viruses are an important component in quantitatively
and qualitatively controlling phytoplankton populations in
natural marine environments.
| |
INTRODUCTION |
Viruses are now recognized as the
most abundant and biologically active components of marine ecosystems
(1, 24). Field studies indicate that the majority are
probably bacterial viruses, i.e., bacteriophages (5, 33),
but viruses and viruslike particles have been observed in many
phytoplankton species and in a wide range of natural seawater samples
(8, 28, 32). These observations have led to increased
interest in the impact of viral infection on the population dynamics
and community structure of marine phytoplankton. Several studies have
suggested that viruses can be significant agents of phytoplankton
mortality. For example, an addition of native virus concentrates
reduced phytoplankton biomass and primary productivity under
experimental laboratory conditions (28, 29). Also, electron
microscopic observations have shown that the proportion of cells
harboring viruslike particles or the abundance of viruslike particles
within the water column increases in the final stages of blooms
(2, 3, 16, 17). In contrast to these postulates, a few
reports have demonstrated that viruses are probably not responsible for
a large proportion of host mortality (33, 36). Waterbury and
Valois (33) observed that some isolated cyanobacteria, Synechococcus spp., tended to be resistant to co-occurring
viruses and concluded that cyanophages were not significant in
controlling host abundance but were likely to influence the clonal
composition of Synechococcus populations in Woods Hole harbor.
Heterosigma akashiwo (Raphidophyceae) is one of the
harmful bloom-forming phytoplankton which often cause mortality of
caged fishes, such as salmon and yellowtail, in coastal waters of
subtropical, temperate, and subarctic areas of the world (10,
27). A noteworthy feature of H. akashiwo
blooms is that they often disintegrate suddenly. Nagasaki et al.
(17) observed by transmission electron microscopy that the
proportion of virus-harboring cells increased along with the sudden
decrease in cell density of H. akashiwo. These data
strongly suggest that viral infection contributes to the disintegration
of H. akashiwo blooms. Recently, lytic viruses infecting H. akashiwo (H. akashiwo virus [HaV]) have been isolated from
natural seawaters and cultured, and their characteristics have
been investigated in the laboratory (18-22). HaV is a
large, double-stranded DNA virus and is most likely specific
for H. akashiwo because the potential for other
phytoplankton species to become infected by this virus has not been
confirmed (18). Other important points are that the
specificity of infection of H. akashiwo is significantly diverse even among HaV clones and that the viral susceptibilities of H. akashiwo isolates can also
be diverse (19, 22). This fact suggests that the interaction
between H. akashiwo and HaV in natural
environments is more than a simple host-virus interaction.
In this study, we monitored the population dynamics of H. akashiwo and HaV during the formation and decay of an
H. akashiwo bloom in Hiroshima Bay, Japan.
Concurrently, a number of H. akashiwo and HaV
clones were isolated and the development in virus susceptibility of the
host species and the host range of the virus were investigated through
laboratory cross-reactivity tests. Our data provide evidence that viral
infection influences the total abundance and the clonal composition of
one host algal species in natural environments.
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MATERIALS AND METHODS |
Sampling.
Surface water was collected from once to three
times a week from a semienclosed basin (Itsukaichi Fishing Port;
34°21.400'N, 132°21.864'E) located in northern Hiroshima Bay, the
Seto Inland Sea of Japan, from mid-May through July 1998. In this area,
an H. akashiwo bloom is an annual event that occurs
around June to July (11). Sampling was conducted between
9:00 and 10:00 a.m. because this species migrates towards the surface
in the early morning (35). Water samples were also collected
from several depths, including 0.2 m above the sediment-water
interface after 3 June.
Abundance of phytoplankton species and lytic viruses.
Cell
counts and taxonomic identification of H. akashiwo
and other phytoplankton species were carried out with a
Sedgewick-Rafter chamber under optical microscopy on the sampling day
without fixation of the sample waters.
The abundance of HaV in seawater was estimated by the most probable
number (MPN) technique (7, 30). Water samples were passed
through a glass fiber filter (Whatman GF/F) and diluted with modified
SWM3 medium (4, 12) in a series of 10-fold dilution steps.
Aliquots (100 µl) of each dilution were added to 8 wells in cell
culture plates with 96 round-bottom wells and mixed with 150 µl of
exponentially growing culture of H. akashiwo. As a
host strain, a clonal strain (H93616) isolated from the northern part
of Hiroshima Bay in June 1993 was used. In previous experiments
(19, 22), this strain was infected and lysed by all HaV
isolates, and we considered it to be the most suitable host strain. The
cell culture plates were incubated under a 14- and 10-h light-dark
cycle of ca. 50 µmol of photons m
2 s1 at
20°C and were monitored for 10 to 14 days for the occurrence of
culture lysis. The abundance of lytic viruses was calculated with a
BASIC program from the number of wells in which lysis occurred (23).
Isolation of H. akashiwo and HaV
clones.
Ten cells of H. akashiwo, as a rule,
were randomly isolated from each water sample on the day of sampling by
the micropipetting method. These clonal but not axenic isolates were
grown in modified SWM3 medium as described above.
One or two HaV clones were isolated from the most diluted wells of each
sample when HaV abundance was determined by the MPN
method. The clonal
isolation was carried out with two cycles of
the extinction dilution
procedure (
6,
18).
Virus susceptibility.
The virus susceptibilities of
H. akashiwo isolates were examined by using a range
of HaV clonal isolates. Each HaV clone was inoculated into a host
culture of the H. akashiwo H93616 strain, and the
resultant fresh lysates were used as inocula. Aliquots (50 µl) of
each lysate were added to 1 ml of exponentially growing culture of each
H. akashiwo isolate. The cultures were incubated under the conditions of light and temperature described above and
monitored for 10 to 14 days for the occurrence of cell lysis. Cultures
that were not lysed 14 days after viral inoculation were considered to
be resistant to the virus clone.
| |
RESULTS |
H. akashiwo dynamics.
On 18 May,
H. akashiwo had already formed a moderate bloom
(8.0 × 103 cells ml1) and maintained
high densities ranging from 6.5 × 103 to 1.4 × 105 ml1 in the surface water from 22 May
through 5 June (Fig. 1a). During this
period, H. akashiwo constituted up to 90% of the
phytoplankton community in terms of cell abundance (data not shown). On
8 June, the cell density of H. akashiwo suddenly
decreased to 3.8 × 102 ml1. This value
is 2 orders of magnitude lower than that on 5 June, indicating that the
bloom disintegrated within a few days. Another interesting observation
was that cells were present at a higher density in the bottom water
than in the surface water on 8 June. This vertical distribution pattern
was the opposite of that during the bloom period. On 1 July,
H. akashiwo exhibited a small peak (2.5 × 103 cells ml1) but did not reach the
densities of a massive bloom formation.
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FIG. 1.
Temporal changes in abundances of H. akashiwo (a) and HaV (b) in surface and bottom waters in
northern Hiroshima Bay, the Seto Inland Sea of Japan, during the period
mid-May to July 1998. Based on the population dynamics of H. akashiwo, the investigation period was tentatively divided
into three periods (I, II, and III).
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With respect to the variability of
H. akashiwo
dynamics described above, we can distinguish three major periods (I,
II, and
III [Fig.
1]). Period I, from 18 May to 5 June, was
characterized
by a dense bloom formation; during period II (from 8 to
25 June),
the bloom disintegrated and the cell density remained at
relatively
low levels; period III, from 1 to 28 July, contained a
smaller
but significant peak, i.e., a secondary
bloom.
Virus dynamics.
Infectious HaV were not detectable (less than
1.3 ml1) in the surface water at the beginning of period
I and were first observed at 102 ml1 on 1 June (Fig. 1b). Coincident with the decline in host abundance, the
concentration of infectious HaV drastically increased and reached
maximum values in both surface (1.9 × 104
ml1) and bottom (1.0 × 106
ml1) waters on 8 June. The latter concentration was
approximately 10 to 100 times higher than the algal abundance in the
surface water during period I. The abundance exponentially decreased
but was present above 102 ml1 in the bottom
water during period II. Despite the significant abundance of
H. akashiwo during period III, the HaV
concentration was extremely low and decreased to a nondetectable level
even in the bottom water by 15 July.
Virus susceptibility and host range.
A total of 89 H. akashiwo isolates were obtained from surface
water during the investigation period. The virus susceptibility of each
isolate was examined against 17 clones of HaV isolated during the same
period. The susceptibility spectra showed various patterns among the
H. akashiwo isolates (Fig.
2). Different spectral patterns were
recognized even among those from the same water sample, indicating that
multiple cells with different viral infection characteristics coexisted
in the water column. There were significant differences in virus
susceptibility (expressed as a percentage of HaV isolates which caused
cell lysis) among H. akashiwo isolates during the
three periods described above. A Kruskal-Wallis test showed that the
susceptibility of H. akashiwo isolates during period II (average ± standard deviation, 18% ± 23%) was
significantly lower than those of isolates during periods I and III
(59% ± 40% and 61% ± 37%, respectively; n = 3; P < 0.001), indicating that H. akashiwo
populations during period II were dominated by cells resistant to the
viruses.
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FIG. 2.
Viral susceptibility spectrum of H. akashiwo isolates to co-occurring HaV isolates from water
samples in northern Hiroshima Bay, the Seto Inland Sea of Japan, during
the period mid-May to July 1998. Both types of isolate are shown in
order of isolation date. Each clonal isolate of H. akashiwo was named according to the isolation date (e.g.,
H98518 was isolated on 18 May 1998), and the number of cultured
isolates obtained from the same water sample is indicated in
parentheses. The shaded and open columns indicate susceptibility (with
cells lysed) and resistance (with cell growth equal to that of the
controls) to each HaV clone, respectively. The roman numerals
correspond to the periods shown in Fig. 1.
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Significant diversity in host ranges was also found among HaV clones
(Fig.
2). Similar to the susceptibility spectra of
H. akashiwo isolates, the host ranges were also slightly
different
even among HaV clones isolated from the same water (HaV25 and
HaV27; HaV36 and HaV37). It was especially remarkable that HaV53,
which
was isolated at the beginning of period III, had a unique
host range.
This virus clone infected and lysed 14 of the 16
H. akashiwo isolates during period II, which was much more
infective
than other HaV clones (which infected only 1 to 4 of the 16
H. akashiwo isolates). In contrast, HaV53 was less
infectious to
H. akashiwo isolates during periods I
and III than the other virus
clones.
| |
DISCUSSION |
Virus impact on host mortality.
In order to measure infectious
HaV abundance, we used the MPN method, in which a single strain of
H. akashiwo (H93616) was used as the host strain.
Titer determination methods (MPN or plaque assay) are the most
sensitive assays for specific viruses in water samples, but their
detection capabilities depend on the host strain used as the assay
organism. Thus, these methods can unpredictably give underestimated
results, especially in a case where different host strains can be lysed
only by selected virus clones. In fact, several studies have found that
the detected viral titers were markedly different depending on the host
strains used (25, 31, 36). Nonetheless, it is most likely
that our MPN assay detected the majority of the infectious HaV in the
water samples, as the host strain we used in this study (H93616) has
been found to be infected and lysed by all HaV clones we have isolated
to date (19, 22).
The data presented in this paper demonstrate that infectious HaV are an
abundant and dynamic component of natural marine environments
and that
their temporal and spatial dynamics are closely related
to host algal
dynamics. The highest concentration of infectious
HaV was found when
the abundance of
H. akashiwo cells suddenly
decreased (Fig.
1). The comparative population dynamics of the
viruses
and the hosts indicate that most of the
H. akashiwo
cells
probably suffered from viral infection and that numerous progeny
viruses were released into the water column by fatal bursting
of the
cells. The vertical distribution pattern of
H. akashiwo cells in the decaying phase of the bloom (period II
[Fig.
1])
also suggests that viral infection was the predominant
factor
in the mortality.
H. akashiwo generally
exhibits diel vertical
migrations characterized by daytime ascent and
dark descent (
27,
35). Actually, in the morning, high
concentrations were observed
in the surface water during the bloom
period (period I). In contrast,
cells were present at a higher
concentration in the bottom water
than in the surface water in the
decaying phase of the bloom (period
II), indicating that most cells
lost their ability to migrate
upward. This was similar to the response
of
H. akashiwo cells
to HaV inoculation under
laboratory conditions; the cells lost
motility within 24 h after
HaV inoculation and consequently sank
to the bottoms of culture vessels
(
21). It has been suggested
that viruses can be significant
agents of phytoplankton mortality
(
2,
3,
16,
17,
24,
26,
28,
29,
32). Most of
the studies were based on transmission electron
microscopic observations
of field-collected phytoplankton cells. For
H. akashiwo, a high
percentage of cells containing
viruslike particles has also been
observed in the final stage of blooms
(
16,
17). However, investigations
of the temporal dynamics
of phytoplankton species and their infectious
viruses in host-virus
systems are scarce (
7,
31,
33,
36).
Bratbak et al.
(
2) showed that the termination of an
Emiliania huxleyi bloom was accompanied by a simultaneous increase in large
viruslike particles in mesocosm experiments. However, there exists
no
direct evidence that these viruslike particles were specific
to
E. huxleyi, although several lines of evidence (e.g.,
morphology
and distribution) suggested that they were probably produced
by
E. huxleyi. As far as we are aware, this is the first
study reporting
a significant inverse relationship between the
abundances of an
algal host and its specific virus in natural seawater,
and it
provides strong evidence that viral infections contribute
greatly
to the disintegration of blooms as mortality
agents.
Viral impact on clonal composition within host population.
Despite the high concentration of infectious HaV, H. akashiwo populations did not completely disappear from the
water column and remained at levels of 101 to
102 cells ml1 during period II (Fig. 1). The
viral susceptibilities of H. akashiwo isolates
indicated that the majority of the isolates during period II were
resistant to most of the HaV clonal isolates (Fig. 2), suggesting that
the H. akashiwo population during period II was dominated by cells resistant to co-occurring viruses. In contrast, the
fact that the viral susceptibilities of the H. akashiwo isolates during period I were much higher than those
during period II suggests that the resistant cells were a minor
component during the bloom period. These observations indicate that the
properties of dominant cells within the H. akashiwo
population change during a period when a bloom is terminated by viral
infection. The development of resistance to viral infection has been
shown to occur in the marine cyanobacteria Synechococcus
spp. (33). Since most Synechococcus isolates were
resistant to co-occurring cyanophages, Waterbury and Valois
(33) concluded that cyanophages were probably not responsible for a large proportion of the cyanobacterial mortality but
were important in determining the clonal composition of these populations. Our data also suggest that viruses can have a significant effect on determining the clonal composition within one host species. However, there is a marked difference between the present study and that of Waterbury and Valois (33). Waterbury and Valois concluded that these cyanobacterial communities are dominated by
cells resistant to their co-occurring phages and that these phages are
maintained by scavenging on the relatively few susceptible cells in the
communities through the annual cycle. In contrast, our data
demonstrated that H. akashiwo populations were
dominated by cells susceptible to viruses and that the resistant cells
were only minor components during the bloom period.
A possible explanation is that host species may pay a cost in reduced
competitive fitness for the increased resistance. It
has been
demonstrated that resistance is often developed through
the alteration
or loss of some important receptor (
13). This
suggests that
resistant cells may confer a competitive disadvantage
against
susceptible ones. Unfortunately there are no studies of
viral
resistance related to physiological strategy for any phytoplankton
species, including
H. akashiwo. Thus, further study
is needed
to explain why
H. akashiwo cells
susceptible to viruses dominated
over the resistant ones during the
bloom
period.
In period III,
H. akashiwo populations were
dominated by cells susceptible to HaV clones again (Fig.
2). One
possibility is
that lytic viruses decreased in abundance. As viruses
must diffuse
randomly from host to host, viral infection is density
dependent
(
15). Thus, a decrease in the abundance of lytic
viruses might
allow the growth of susceptible cells. Another
possibility is
that the resistant cells which dominated during period
II might
also be infected and lysed by viruses. Indeed, the virus clone
HaV53 infecting these resistant cells was isolated from the water
sample at the beginning of period III. This also shows that natural
H. akashiwo populations do not consist simply of
two distinct
groups, i.e., susceptible and resistant groups, suggesting
that
the relationship between
H. akashiwo and HaV
in natural environments
is very
complex.
Implications.
Our data provide evidence that viral infection
influences not only the total abundance but also the clonal composition
of one host algal species in natural seawater. This leads us to propose a hypothetical model describing interactions between one host algal
species and its infectious viruses (Fig.
3). In this model, it is assumed that
there are two distinct subpopulations (A and B) with different viral
infection characteristics within one phytoplankton species and that
viruses 
A and B specifically infect subpopulations A and B,
respectively. Under favorable growth conditions for one subpopulation
(A), subpopulation A quickly increases in population density and
subpopulation B remains at a low level of abundance. If no viral
infection occurs, subpopulation A maintains dominance and eventually
will eliminate subpopulation B. On the other hand, the presence of
virus A specifically decreases subpopulation A, and subpopulation B,
which is resistant to virus A, then dominates. Consequently, the
total host abundance decreases but subpopulation succession occurs, and
the clonal diversity within one phytoplankton species is maintained
under constant environmental conditions. We acknowledge that this
conceptual model oversimplifies the very complex series of
host-virus interactions in natural environments. Nonetheless, the model
is useful in generalizing viral impacts on the total abundance and
strain composition of one host algal species on the basis of the data
on the temporal dynamics of H. akashiwo and its
infectious viruses empirically obtained in the present study.
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FIG. 3.
Conceptual model describing interactions between one
host algal species and its infectious virus. The model hypothesizes
changes in the total abundance and clonal composition of one host algal
species in response to viral infection. It is assumed that there are
two distinct subpopulations (A and B) with different viral infection
characteristics within one phytoplankton species and that viruses A
and B specifically infect subpopulations A and B, respectively. For
a detailed explanation, see Discussion.
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It has been demonstrated that some procaryotic and eucaryotic
phytoplankton species comprise genetically and/or physiologically
different strains (
9,
14). Although we do not have any
information
about the genetic and/or physiological differences
among
H. akashiwo cells, the diversity of their
viral susceptibilities probably
reflects some genetic or
physiological differences. Therefore,
viral infection may
contribute to the maintenance of genetic and
physiological diversity
within one phytoplankton species. Moreover,
as genetic and
physiological diversity presumably allows populations
to thrive
under a broad range of environmental conditions, viral
infection might
function as an advantageous strategy in the ecological
success of a
host
species.
| |
ACKNOWLEDGMENTS |
This work was supported by grants from the Fisheries Agency of
Japan and from the Japan Science and Technology Corporation.
We thank K. Tamai (National Research Institute of Fisheries and
Environment of Inland Sea) for many helpful comments on the manuscript.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Harmful Algal
Bloom Division, National Research Institute of Fisheries and
Environment of Inland Sea, 2-17-5 Maruishi, Ohno, Saeki, Hiroshima
739-0452, Japan. Phone: 81-829-55-0666. Fax: 81-829-54-1216. E-mail: nagasaki{at}nnf.affrc.go.jp.
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Applied and Environmental Microbiology, November 2000, p. 4916-4920, Vol. 66, No. 11
0099-2240/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
