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Phycology |
2School of Biology and Biochemistry, Queen's University, Medical Biology Centre, 97 Lisburn Road, Belfast BT9 7BL, Northern Ireland, UK; 3Finnish Environment Institute, P.O. Box 140, 00251 Helsinki, Finland; 4Department of Microbiology, P.O. Box 56, University of Helsinki, 00014 Helsinki, Finland
Received for publication August 28, 2001. Accepted for publication May 31, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Baltic Sea • Chlorophyta • Enteromorpha intestinalis • green tides • ITS sequences • monostromatic • morphology • phylogenetic analysis • Ulvophyceae
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Fletcher, 1996
; Hernández et al., 1997
; Valiela et al., 1997
; Raffaelli, Raven, and Poole, 1998
). Astonishing quantities of material (up to 27 kg wet mass/m2) are cast up or drift in shallow water, constituting a major nuisance in sheltered bays around the world (Fletcher, 1996
). Deleterious ecological effects include the uncoupling of biogeochemical cycles in sediments from those in water columns (Valiela et al., 1997
), a negative impact on seagrass beds due to shading, and disruption of feeding by wading birds (Raffaelli, Raven, and Poole, 1998
). The costs of mitigation are high, involving the removal of about 108 kg of seaweed per annum from recreational beaches of Atlantic France alone (Dion and Le Bozec, 1996
). Because of their economic impact, green tides have been the focus of a large number of ecological studies in Europe, North America, and Australia (reviewed by Fletcher, 1996
; Valiela et al., 1997
; Raffaelli, Raven, and Poole, 1998
).
The great majority of blooms are reported to consist of members of just two genera of the Ulvophyceae, Ulva and Enteromorpha (Fletcher, 1996
). These are among the world's most common fouling algae, which are used as model organisms in studies of spore bioadhesion (Stanley, Callow, and Callow, 1999
; Callow et al., 2000
). Their life histories consist of morphologically similar haploid and diploid phases, both of which reproduce prolifically by haploid or diploid asexual zoospores formed by mitotic division of vegetative cells (van den Hoek and Mann, 1996
). Sexual reproduction involves fusion of opposite mating types of haploid gametes, which can also develop parthenogenetically into adult thalli. Ulva and Enteromorpha differ markedly in their general morphology (flat bilayered blades vs. hollow tubes a single cell in thickness; Burrows, 1991
). Although molecular phylogenetic analysis has recently revealed that the two genera are not distinct evolutionary entities (Tan et al., 1999
), both names are used here pending taxonomic revision.
A better understanding of the origin and persistence of green tide blooms is desirable in order to address the problems they cause. Even simple taxonomic identification is confounded because the unattached algae are often morphologically atypical (Malta, Draisma, and Kamermans, 1999
). As yet there have been very few studies concerning any aspects of the molecular ecology of green tides. However, in conjunction with life-history studies, use of appropriate molecular markers can both identify the algae and provide important information concerning the origins and dynamics of the blooms (Coat et al., 1998
; Malta, Draisma, and Kamermans, 1999
). Such information is required to inform management decisions. Proposed remediation measures typically involve altering "bottom-up" controls, i.e., reducing nutrient supply (Valiela et al., 1997
).
The Baltic Sea, because of its enclosed nature, is prone to eutrophication that has favored the formation of green tides. The Gulf of Finland is one of the most eutrophic areas (Lappalainen and Pönni, 2000
), receiving 76 x 105 kg of phosphorus and 138 x 106 kg of nitrogen annually (Pitkänen et al., 1998
). A green tide has occurred there over a large area on the west coast of Finland every summer between 1992 and 2000. This bloom consists of free-floating single-layered sheets that superficially resemble Monostroma, a genus of the Codiolales (Ulvophyceae) not closely related to Ulva and Enteromorpha (Ulvales) and rarely regarded as a green tide-forming green alga (Fletcher, 1996
).
To resolve the identity of this morphologically unusual bloom and, if possible, determine its origins, we made comparative analyses of rDNA internal transcribed spacer 1 (ITS1) and ITS2 spacers and the 5.8S gene. This molecular marker was chosen because ITS sequences are available for a large number of green algal species, including several that form green tides, and can often reveal microevolutionary processes (Blomster, Maggs, and Stanhope, 1998
, 1999
) as well as providing definite taxonomic identification (Blomster, Maggs, and Stanhope, 1998
, 1999
; Coat et al., 1998
; Tan et al., 1999
; Blomster et al., 2000
). We also sought by culture studies to determine the life history of this bloom-forming alga and examine whether its unusual morphology might be linked to the green tide environment.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The salinity is 4–5 practical salinity units (PSU) throughout the year in this tideless area. During the winter, ice cover of up to 1 m can last for a maximum of 4 mo, and algal distribution in winter was surveyed by dredging through holes drilled through the ice.
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). When unialgal, as determined by careful microscopic examination, isolates were grown in enriched artificial seawater in 50-mL tissue culture bottles, with a monthly change of medium, under standard conditions of 15°C in a 12 h light : 12 h dark photoperiod. In attempts to induce reproduction, a series of transfers between a wide range of culture conditions was undertaken. All aspects of the culture environment were varied sequentially. First, the enriched medium was replaced with autoclaved 5–6 PSU sea water without nutrient additions, then the salinity was reduced by using autoclaved tap water. The temperature was changed to 5°, 10°, 15°, or 20°C, and the daylength was changed from 12 h : 12 h to 18 h : 6 h. Desiccation of the sheets under damp conditions was followed by rehydration in medium. The final culture treatment involved leaving the medium unchanged for 2 mo, then replacing it, which induced new growth that was transferred to fresh bottles. Following the discovery that the monostromatic sheets could give rise to thalli resembling Enteromorpha intestinalis, attached E. intestinalis thalli were collected from Hanko, Tvärminne, Finland (59°50' N; 24°15' E) in September 1995 and from Espoo, Haukilahti, Finland (60°10' N; 24°45' E) in April 1996. Cultures were grown under the standard conditions described above.
Cultured material for DNA extraction was preserved in silica gel; subsamples were pressed for herbarium specimens and photographed. Voucher specimens were prepared and deposited in the Ulster Museum, Belfast (F11947), and the Natural History Museum, London, UK.
DNA extraction and sequencing
DNA of the monostromatic sheets was extracted from silica gel-preserved tissue of three individual thalli collected in June 1997 and from a culture. Other algal material for DNA extraction was collected from various locations in the Atlantic and the Baltic. Collection data and GenBank accession numbers can be found at the AJB Supplementary Data web site (http://ajbsupp.botany.org/v89/). Fifty-milligram samples were ground to a fine powder in liquid nitrogen and DNA was phenol chloroform extracted using a modified total genomic DNA extraction protocol for algal material (Blomster, Maggs, and Stanhope, 1999
). Polymerase chain reaction (PCR) amplification and sequencing of the ribosomal DNA cistron including the complete ITS1, 5.8S, and ITS2 regions were performed using primers described in Blomster, Maggs, and Stanhope (1998)
. The PCR-amplified products were directly sequenced using dideoxy chain-termination methodology with dye-termination reactions of 30 pmol primer and 400 ng template DNA in 20 µL reactions. The cycle sequencing reactions were carried out in a cycle of initial denaturation at 96°C for 1 min, followed by 25 cycles of 96°C for 50 s, 62°C for 4 min, and 50°C for 20 s. The reactions were loaded on Perkin-Elmer ABI 373A or ABI 377 automated sequencers. The cistron was sequenced on both strands with each reaction repeated at least three different times in different sequence runs.
Data analysis
The ITS1, ITS2, and 5.8S sequences were aligned with 21 sequences of other monostromatic sheets (Monostroma grevillei), distromatic sheets (Ulva species), and tubular green algae (Enteromorpha species). The sequence alignments were constructed using ClustalW Multiple Alignment option (Thompson, Higgins, and Gibson, 1994
) within the BioEdit Sequence Alignment Editor 4.8.10. The alignment was perfected by eye using BioEdit (Hall, 1999
). Because of the high sequence divergence in some parts of the alignment between different genera in the study, only the most conserved regions (506 base pairs [bp] of the total 610 bp) were included in this analysis. The data were analyzed using maximum parsimony (MP), neighbor-joining (NJ), and maximum-likelihood (ML) methods with PHYLIP 3.5c (Felsenstein, 1993
). The robustness of the MP and NJ phylogenetic hypotheses was tested by bootstrapping (Felsenstein, 1985
) with 1000 replications of the data. The number of most parsimonious trees was determined by randomizing the input order ten times. The distance matrix, also used for NJ analysis, used maximum likelihood distances with a transition : transversion ratio of 2.0 and empirical base frequencies. Determination of the highest likelihood tree was made with the expected transition : transversion ratio at 2.0. A significance test was carried out between a user-defined constrained tree and the MP tree using the method proposed by Templeton (1983)
. All trees were unrooted, because the taxa included are so distantly related that potential outgroup sequences could not be aligned with them. For examination of the relationships among samples of Enteromorpha intestinalis, a complete alignment of all E. intestinalis sequences was constructed.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). They persisted throughout the entire year in small quantities and survived for 4 mo under the ice as small fragments.
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Attached E. intestinalis collected from two localities in Finland always sporulated freely under the standard culture conditions, producing abundant viable spores. In most cases virtually the whole thallus was converted into spores after a relatively short cultivation period.
Phylogenetic analyses
The sequence alignment of 506 bp contained 254 variable sites. The most likely ML tree (Ln likelihood = –2774.0) supported the monophyly of sheet-like samples (including the tubular culture) and E. intestinalis samples (Fig. 5). In the parsimony analysis 89 most parsimonious trees (MPTs) of length 575 steps were found. In all of these trees the field-collected sheet-like samples and the cultured tubular thalli were grouped with E. intestinalis samples from the Baltic and Atlantic and separated from the Monostroma samples, Ulva samples, and other Enteromorpha samples. Bootstrap support for the assemblage of the sheet-like algae, including their tubular derivatives, and E. intestinalis samples was 98% (NJ) to 100% (MP) (Fig. 5). A user-defined tree that constrained the monophyly of all monostromatic sheets, i.e., grouped the Baltic sheet-like samples with Monostroma, added 27 steps to the MPT. It was 702 steps in length and was significantly longer than the most parsimonious trees.
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) and two transversions (both C to T) for Baltic 1 and Ireland 611. There were no unique synapomorphies for the four bloom sequences (monostromatic sheets and tubular culture). Sheet 1 differed at both putative microsatellite loci from sheets 2 and 3.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Sequence divergence of 0–2.2% among E. intestinalis samples is comparable to the levels found within other monospecific groupings in the Ulvales, such as Atlantic E. compressa (0–2.3%; Blomster, Maggs, and Stanhope, 1998
; Tan et al., 1999
) and E. muscoides (0–0.6%; Blomster, Maggs, and Stanhope, 1999
). Blooms of single-layered sheet-like green algae observed in the Baltic Sea have previously been identified as members of the genus Monostroma in the Codiolales, not closely related to Ulva and Enteromorpha (Ulvales). At Inre Verkviken in the northern Aland Islands, such loose-lying sheets were attributed to Monostroma balticum (Mathiesen and Mathiesen, 1992
), whereas in the Askö area of eastern Sweden similar springtime blooms were identified as Monostroma grevillei (Wallentinus, 1976
, p. 98, 1979
). It is possible that Monostroma does form blooms in the Baltic, but previous reports may represent misidentifications of E. intestinalis based on the aberrant morphology. Taxonomic identification has important implications for understanding the dynamics of these green tides, because the haplo-diploid life history of Monostroma involves a microscopic "codiolum" phase that grows endophytically within other algae, in contrast to the isomorphic life history of Ulva and Enteromorpha.
Origin and persistence of the bloom
With the exception of mononucleotide repeats, all four sequences of the bloom-forming Baltic E. intestinalis were identical. Substitutions associated with two probable microsatellite mononucleotide repeats are likely to be phylogenetically misleading, because such loci exhibit high levels of bidirectional mutation and hence homoplasy (Provan, Powell, and Hollingsworth, 2001
). Published 5.8S gene sequences for attached Baltic populations of E. intestinalis, including three samples from southwestern Finland, exhibited two unique T to G transversions (Fig. 6; Leskinen and Pamilo, 1997
). We could infer from this that the blooms were not derived from attached populations at nearby sites. However, these positions are otherwise invariant in a large alignment of green algal 5.8S sequences (H. Hayden, University of Washington, unpublished data). As T to G is the rarest nucleotide substitution (Nei and Kumar, 2000
) and compressions due to GC-rich template DNA almost invariably lead to incorrectly determined Gs, sequencing error may be involved. If this is taken as a working assumption, and putative microsatellite variation is ignored, sequences of our bloom-forming E. intestinalis correspond to Leskinen and Pamilo's (1997)
haplotype 2. Even when the mononucleotide repeats are included, the ITS1 and ITS2 sequences for two of the three bloom samples were identical to their haplotype 2, which was obtained from three sites in southwestern Finland, as well as in Sweden. The ITS1 and ITS2 sequences of Leskinen and Pamilo's (1997)
haplotype 1, which they found only in Swedish samples, were identical to one of our Atlantic sequences (611) from a freshwater stream in Ireland.
The identical ITS1 and ITS2 sequences of bloom-forming E. intestinalis and attached populations in southwestern Finland are consistent with the bloom having originated from typical tubular thalli that occur in the local area (Keskitalo and Ilus, 1987
), rather than by introduction of an existing sheet-like form from a different geographical area. This is also supported by our findings that the thalli derived from isolated cells of the sheets were hollow tubular plants. We found no evidence that sheet-forming E. intestinalis reproduces by spores, either in the field or in culture, unlike the attached populations. Instead, the presence of small fragments throughout the winter shows that the bloom persists vegetatively and reproduces by fragmentation. Monostromatic sheets may originate infrequently from attached tubular thalli, then reproduce clonally. Survival in a culture of a few cells in otherwise dead thalli ("propagules") has previously been observed in E. intestinalis (Burrows, 1959
). She showed that this was an effective method of vegetative propagation in conditions unfavorable for the survival of delicate zoospores, such as extreme cold or marked salinity changes. Normal tubular thalli were never observed in association with the monostromatic sheets under the Baltic bloom conditions. In culture, however, once tubular thalli had formed by regeneration, they did not revert to the monostromatic sheet form.
A similar situation was found in the Veerse Meer (Netherlands), where unattached green tide Ulva scandinavica populations very rarely reproduce by spores. Instead they overwinter buried in the sediment (Kamermans et al., 1998
; Malta, Draisma, and Kamermans, 1999
), which is consistent with a rare origin of the blooms from attached populations. For the blooms in Finland and the Netherlands, removal of biomass might therefore be an appropriate "top-down" mitigation measure. In contrast, in Brittany, France, green tides and local attached populations of Ulva armoricana reproduced freely by spores (Coat et al., 1998
; Dion, de Reviers, and Coat, 1998
). The planktonic spore stage in their life history makes them vulnerable to benthic filter feeders; Ruiz (1999)
has presented evidence to suggest that such green tides can be reduced by high densities of cultured oysters.
Green tides and morphological plasticity in the Ulvales
Flexibility of form in Enteromorpha intestinalis, such as the formation of branches in normally unbranched plants, has long been recognized (Reed and Russell, 1978
). However, this is the first report of a monostromatic morph in this genus despite numerous physiological and ecological studies (Poole and Raven, 1997
). Aberrant phenotypes of green algae are frequently associated with green tides. In the Veerse Meer, three different morphological species of Ulva were shown to have been induced in conspecific samples (Malta, Draisma, and Kamermans, 1999
). Tan et al. (1999)
collected distromatic sheet-like Ulva pseudocurvata samples from a 4 km long estuary in Aberdeenshire, Scotland, characterized by extensive green tides (Raffaeli, Raven, and Poole, 1998
). These samples formed a strongly supported clade with samples of tubular E. compressa (Fig. 5). The sequence divergence within this clade ranged from only 0.42% to 1.7%, comparable with levels within other monospecific groupings of Enteromorpha and Ulva. Partly distromatic unbranched Enteromorpha linza and highly branched tubular E. procera samples with very different morphologies were likewise closely related (Tan et al., 1999
).
Morphological changes in green algae are induced by altered nutrient supply in eutrophicated conditions (Valiela et al., 1997
), as well as by salinity changes (Reed and Russell, 1978
). Aberrant growth forms are believed to have better potential for survival in the prevailing conditions (e.g., rapid nutrient uptake when only one cell layer thick, with a high surface-to-volume ratio; Valiela et al., 1997
). This may also explain in part why Enteromorpha and Ulva remain the main components of green tides (Poole and Raven, 1997
). This novel morphology of E. intestinalis indicates that the contribution of this species to biofouling and green tides may have been underestimated previously. Further work is needed to establish the causal relationship between green tide conditions and radical changes in morphology in E. intestinalis. Accurate identification of the causal agents of green tides is an essential prerequisite to understanding the processes that contribute to green tides, particularly as increasing pressure on coastal marine environments could result in further novel forms in this morphologically plastic green algal species.
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FOOTNOTES |
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5 Current address: Division of Systematic Biology, P.O. Box 7, University of Helsinki, 00014 Helsinki, Finland
6 Author for reprint requests (c.maggs{at}qub.ac.uk
)
7 Current address: Bioinformatics, GlaxoSmithKline, 1250 S. Collegeville Road, Collegeville, PA 19426, USA
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Blomster J. E. M. Hoey C. A. Maggs M. J. Stanhope 2000 Species-specific oligonucleotide probes for macroalgae: molecular discrimination of two marine fouling species of Enteromorpha (Chlorophyceae). Molecular Ecology 9: 177-186[CrossRef][Medline]
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Blomster J. C. A. Maggs M. J. Stanhope 1999 Extensive intraspecific morphological variaton in Enteromorpha muscoides (Chlorophyta) revealed by molecular analysis. Journal of Phycology 35: 575-586[CrossRef][ISI]
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