Review Article
Putting the C in phycology
- JOHN A. RAVEN
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- 01 November 1997, pp. 319-333
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This article considers molecular biological to global environment work on inorganic carbon acquisition processes in the algae sensu lato (i.e. including the cyanobacteria).
At least 95% of the organic C in photolithotrophic algae has been fixed by RUBISCO, while the remaining 5% or so has involved a range of anaplerotic carboxylases. The catalytic characteristics of RUBISCO show substantial phylogenetic variation; for some algal RUBISCOs (those from cyanobacteria and, possibly, Dinophyta) the kinetics of the carboxylase and oxygenase activity are such that net photosynthetic CO2 fixation could not occur with diffusive CO2 entry from air-equilibrium solution. In many other algae the kinetics of inorganic C assimilation are at variance with in vitro RUBISCO kinetics, and, as in cyanobacteria and Dinophyta, a CO2-concentrating mechanism is hypothesized. In many cases, the operation of such a mechanism can be demonstrated as a higher internal than external CO2 level during photosynthesis. In cases where such a CO2 concentration difference cannot be demonstrated, mechanisms may produce CO2 from HCO3− in an extracellular or intracellular compartment maintained at a lower pH than the cytosol and stroma but, with the exception of the acid zones on the surface of certain characeans, such mechanisms have not been experimentally verified. Reactions downstream of RUBISCO include the polyphyletic metabolic processes which deal with the products of RUBISCO oxygenase activity subsequent to phosphoglycolate phosphatase; even when a CO2-concentrating mechanism is present there is a minor C flux through phosphoglycolate. There are important consequences for bioenergetics, for the allocation among solutes of the low intracellular osmolarity of some freshwater algae, and of the occurrence of CO2-concentrating mechanisms or of diffusive CO2 entry. Some algae today are inorganic C-limited for photosynthesis in their natural environment under otherwise optimal conditions; even in these organisms it is not clear that they are C-limited in nature. The chances of C limitation in the past would have been greater with the low CO2 concentrations of the last glacial maximum 18,000 years ago, but would have been less likely to be C limited in the pre-pleistocene past, and in the anthropogenically CO2-enriched future, than at present. The evaluation of inorganic C acquisition mechanisms must be viewed against the general decrease in CO2, and increase in O2, over the almost 4 billion years since RUBISCO-based CO2 fixation evolved. It is not yet clear whether (polypheletic) CO2 concentrating mechanisms or (polyphyletic) mechanisms of glycolate metabolism evolved first.
Research Article
Strategies of adaptation by Antarctic cyanobacteria to ultraviolet radiation
- A. QUESADA, W. F. VINCENT
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- 01 November 1997, pp. 335-342
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Effects of UVA and UVB radiation were evaluated on two cyanobacterial strains (Phormidium murrayi and Oscillatoria priestleyi) isolated from the McMurdo Ice Shelf, Antarctica. The two isolates showed some similarities, but also major differences in their qualitative and quantitative responses to ultraviolet radiation (UVR). Growth decreased with increasing UVR, but with a 5-fold (UVA) or 10-fold (UVB) greater effect on O. priestleyi than P. murrayi. In both isolates, cellular concentrations of phycobiliproteins (measured by in vivo absorbance), and to a lesser extent chlorophyll a, diminished with increasing UVR exposure. Spectral scans of methanol extracts indicated the presence of UVR-screening compounds in O. priestleyi but not P. murrayi; however, the absorbance per unit dry weight was low, and similar in cultures with and without UVR. Carotenoid pigments increased up to a threshold UVB flux and thereafter decreased. In both isolates, moderate UVA lessened the effect of growth inhibition by UVB, consistent with a UVA-activated repair mechanism. Comparative motility tests showed that O. priestleyi is a fast gliding species that can rapidly relocate in response to changes in ambient light, while P. murrayi is non-motile. The ability of O. priestleyi to escape UVR by gliding, and the greater ability of P. murrayi to tolerate UVA and UVB exposure, illustrate the differences in UVR survival strategies even between closely related species of cyanobacteria.
Molecular systematics of the Gelidiales: inferences from separate and combined analyses of plastid rbcL and nuclear SSU gene sequences
- J. CRAIG BAILEY, D. WILSON FRESHWATER
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- 01 November 1997, pp. 343-352
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Nucleotide gene sequences for both the nuclear-encoded small-subunit RNA (SSU) and plastid-encoded large subunit of RuBisCO (rbcL) were determined for 16 species classified in the red algal order Gelidiales. Sequence comparisons indicate that rbcL is evolving at a faster rate than SSU in these species and that there is a more even distribution of changes across the length of the rbcL gene compared with that observed for the SSU gene. The rbcL sequences also showed a marked anti-GC bias at synonymous third-codon base positions. Parsimony and maximum-likelihood analyses were used to generate phylogenetic trees from both separate and combined analyses of the two sequence data sets. Relationships among most taxa are resolved robustly; however, the relative order of branching for the Capreolia and Ptilophora clades remains uncertain. The molecular data provide unambiguous, independent support for recognition of the newly established genus Pterocladiella. Although the position of Pterocladiella within the Gelidiales was not resolved clearly by the rbcL data alone, analyses of both the SSU and combined data matrices indicate that this genus is one of the three earliest-diverging lineages within the order. These data also suggest that Gelidium as currently circumscribed is not monophyletic. Molecular and morphological evidence suggests that the origin and, perhaps, diversification of the major lineages of gelidialean algae is correlated with distinct, independently evolved nutritional strategies for the developing carposporophyte.
Changes in the diatom community, including the appearance of Actinocyclus normanii f. subsalsa, during the biomanipulation of Lake Vesijärvi, Finland
- MIKKO LIUKKONEN, TIMO KAIRESALO, ELIZABETH Y. HAWORTH
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- 01 November 1997, pp. 353-361
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After 60 years of receiving treated sewage effluent from the city of Lahti, Lake Vesijärvi had become very eutrophic. Diversion of the effluent in 1976 resulted in a slow recovery of the water quality. In 1989–93, biomanipulation removed 380 kg of coarse fish per hectare from Enonselkä, the most polluted basin of the lake. Since then cyanobacterial blooms have decreased and water transparency has increased. Paleolimnological analysis of deep water sediments was used to reconstruct the changes in the diatom community, with varved sediment structure providing a year-by-year chronology. During the biomanipulation period the following diatom species increased in Enonselkä: Asterionella formosa, Fragilaria crotonensis, Stephanodiscus heterostylus and Tabellaria spp. In contrast, diatom species commonly considered to be indicators of eutrophication, such as Aulacoseira islandica, Diatoma elongatum and Stephanodiscus parvus, have decreased since the end of the 1980s reflecting the recovery of the Enonselkä basin. The changes in the diatom plankton recorded in the less polluted basin of Laitialanselkä were much less marked than those recorded from the sediments of the Enonselkä basin. In 1990 a diatom species, Actinocyclus normanii f. subsalsa, appeared for the first time in Lake Vesijärvi and since then it has been one of the dominant diatoms in the plankton of the Enonselkä basin. Two years later it was also present in small numbers in the plankton of Laitialanselkä, the least polluted basin of the lake. The appearance of A. normanii f. subsalsa was concomitant with the dredging of the boat harbour of Lahti city in the late summer of 1990. It was therefore apparently not directly affected by biomanipulation but benefited indirectly from the collapse of cyanobacterial populations that led to improved light and nutrient availability in the water column.
Daily course of photosynthesis and photoinhibition in Chondrus crispus (Rhodophyta) from different shore levels
- S. SAGERT, R. M. FORSTER, P. FEUERPFEIL, H. SCHUBERT
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- 01 November 1997, pp. 363-371
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Photoinhibition of photosynthesis in the red alga Chondrus crispus from different shore levels was investigated under laboratory and field conditions. The underwater light climate at Roscoff (French Atlantic coast), characterized by transmittance spectra, was shown to be intermediate between Jerlov coastal type 1 and oceanic type III. Chondrus crispus thalli were collected at four depths (3·5–8·5 m below high tide level) and exposed to daily courses of artificial and natural light. Filters were used to discriminate between the effects of photosynthetically active radiation (PAR) and ultraviolet radiation (UVR) under the photoinhibitory treatments. In the presence of natural UVR, photoinhibition at midday was increased by up to 60%. Recovery from photoinhibition was measured at different times throughout the light stress. Recovery kinetics differed between morning and early afternoon in all treatments, and were dependent on the light dose. Whereas biphasic kinetics were observed in all treatments in the morning, the recovery in early afternoon was significantly slower. The influence of UVR on recovery was apparent after exposure to higher light doses. In all investigations, sensitivity to photoinhibition corresponded to zonation of the algae, with deeper-growing algae showing a greater depression of fluorescence yield, and slower recovery (indicating acclimation to the growth irradiance). An increase in the phycoerythrin content and increasing photosynthetic efficiency with increasing growth depth were observed.
A comparison of fermentation in the cyanobacterium Microcystis PCC7806 grown under a light/dark cycle and continuous light
- ROY MOEZELAAR, LUCAS J. STAL
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- 01 November 1997, pp. 373-378
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The cyanobacterium Microcystis PCC7806, grown under continuous light, fermented endogenously stored glycogen to equimolar amounts of acetate and ethanol when incubated anaerobically in the dark. In addition, H2, CO2 and some L-lactate were produced. This fermentation pattern differed from that displayed by cells which had been grown under an alternating light/dark (16/8 h) cycle. Such cells produced much more ethanol than acetate, while no lactate was formed. These differences could not be related to the levels of key enzymes of fermentation, which were identical in the two cultures. The cultures grown under continuous light contained twice as much glycogen as the light/dark-grown cells and the former metabolized it at a rate approximately 3 times as fast as the latter culture. Fermentation in the culture grown under continuous light showed low carbon recovery (59–80%) and high oxidation/reduction balance (approximately 1·5). On the basis of calculations of ATP yield it was concluded that this culture was capable of growth driven by fermentation. The increase in structural cell material would account for the missing carbon and reduction equivalents.
Inter- and intraspecific genetic variation in Caulerpa (Chlorophyta) based on nuclear rDNA ITS sequences
- A. PILLMANN, G. W. WOOLCOTT, J. L. OLSEN, W. T. STAM, R. J. KING
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- 01 November 1997, pp. 379-386
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Caulerpa (Chlorophyta, Ulvophyceae) is a common marine tropical-subtropical genus of about 70 species, inhabiting the eulittoral zone on rocks and corals as well as mangroves. The genus is particularly diverse and abundant along southern Australian coasts, where it is thought to have originated. Here, we compare sequences from the nuclear ribosomal cistron among five species of Caulerpa, including nine populations of Caulerpa filiformis from two biogeographic regions: five from Australia and four from South Africa. Species relationships were well resolved by internal transcribed spacer (ITS) sequences and supported by high bootstrap values as follows: (C. geminata (C. simpliciuscula (C. trifaria (C. scalpelliformis (C. filiformis – Australia, C. filiformis – South Africa))))). Nucleotide divergence within C. filiformis was low with four and five nucleotide differences present in ITS1 and ITS2 respectively. Unexpectedly, the 5.8S rRNA gene showed eight nucleotide differences between the Australian and South African populations and may indicate cryptic species. The Australian C. filiformis is probably not a South African introduction. These sequences provide an independent means for assessment of species relationships and appear, in so far as limited taxon sampling permits, to follow chloroplast ultrastructural groupings proposed 20 years ago.
Secondary carotenoid accumulation in flagellates of the green alga Haematococcus lacustris
- KAY GRÜNEWALD, CHRISTOPH HAGEN, WOLFRAM BRAUNE
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- 01 November 1997, pp. 387-392
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The combination of nitrogen deprivation and increased cultivation light intensity resulted in the synthesis of secondary carotenoids in flagellates of Haematococcus lacustris. The pigment pattern was characterized by high-pressure liquid chromatography analysis during the accumulation period and in response to inhibitors of carotenoid biosynthesis (diphenylamine, norflurazon and tetcyclacis). Diphenylamine treatment resulted in (i) a decrease in ketocarotenoids and (ii) an accumulation of β-carotene and zeaxanthin due to inhibition of the β-carotene oxygenase. Our results indicate that astaxanthin synthesis in H. lacustris follows the biosynthetic pathway elucidated in the marine bacterium Agrobacterium aurantiacum.
The identification of Chrysochromulina and Prymnesium species (Haptophyta, Prymnesiophyceae) using fluorescent or chemiluminescent oligonucleotide probes: a means for improving studies on toxic algae
- NATHALIE SIMON, JOACHIM BRENNER, BENTE EDVARDSEN, LINDA K. MEDLIN
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- 01 November 1997, pp. 393-401
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Chrysochromulina and Prymnesium are important bloom-forming organisms in marine and brackish waters, respectively. Both genera include toxic species, which are primarily implicated in fish kills. Previous analyses of small subunit (SSU) rDNA sequences from Chrysochromulina and Prymnesium spp. indicate that Chrysochromulina is paraphyletic. C. polylepis, which produced a spectacular, harmful bloom in 1988, is more closely related to toxic Prymnesium species than to most other Chrysochromulina species based on rDNA sequence comparisons. Signatures were identified in the SSU rRNA gene specific for a clade that comprised primarily toxic taxa (C. polylepis, P. parvum, P. patelliferum and P. calathiferum) and that recognized C. polylepis alone. Oligonucleotide probes complementary to these regions were designed, and their specificity tested using dot-blot hybridization on PCR products of the SSU rRNA gene from 28 strains of Chrysochromulina and Prymnesium. Whole-cell hybridizations were performed with FLUOS- as well as Cy3-labelled probes on cultured species from both genera, and were detected with both epifluorescence microscopy and flow cytometry. The probes afforded easy identification of clonal isolates of C. polylepis and a cluster of closely related species including C. polylepis and Prymnesium spp. The feasibility of using these probes for species identification and studies of population dynamics in the field is discussed.
Deep-layer autotrophic picoplankton maximum in the oligotrophic Lake Stechlin, Germany: origin, activity, development and erosion
- JUDIT PADISÁK, LOTHAR KRIENITZ, RAINER KOSCHEL, JIRÍ NEDOMA
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- 01 November 1997, pp. 403-416
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Autotrophic picoplankton (APP) abundance, primary production and vertical distribution were studied in the oligotrophic Lake Stechlin (northeastern Germany) in 1994 and 1995. Within the euphotic zone APP contributed 34% of phytoplankton biomass and 35% of primary production. Annual average APP cell number was 209×103 cells ml−1, of which 95% were unicellular cyanobacteria, 2% were colonial cyanobacteria and 3% were eukaryotes. Three ecologically and/or morphologically different groups of APP were recognized: (i) unicellular cyanobacteria belonging to the genus Cyanobium, (ii) eukaryotic species growing in early spring under isothermal conditions and (iii) cyanobacteria, partly colonial species, growing in the stratified period in the euphotic zone. Three species of eukaryotic green algae were identified: Choricystis minor, Neocystis diplococca and Pseudodictyosphaerium jurisii, the latter two being colonial. This is the first record of the occurrence of colonial eukaryotes potentially of APP size in fresh waters. In summer picocyanobacteria were highly productive so the low net increase rates indicate that losses must be high. The dominant, Cyanobium population started growing in February with maximum abundance in late April, contributing significantly to the spring peak in phytoplankton biomass. During this growth period, the population was evenly distributed in the 60 m water column. By the time the maximum biomass occurred, inorganic nutrients had decreased below analytically detectable levels. Parallel to the onset of stratification a part of the population was grazed, most probably in the microbial loop and primarily in the upper 10–15 m. The rest of the Cyanobium population accumulated in a narrow layer in the upper hypoliminon. The APP remaining from the spring was persistent for much of the summer in this cold, high-nutrient (especially nitrate)/low-light environment. Short phosphorus-turnover times suggest that APP is probably phosphate-limited. The stability of the thermocline and the pattern of thermocline development in May affected the accumulation of the APP cells in the upper hypolimnion. Thus, this process is sensitive to the physical stability of the water column.
Photocontrol of short-term growth in Porphyra leucosticta (Rhodophyta)
- JOSÉ AGUILERA, FÉLIX L. FIGUEROA, F. XAVIER NIELL
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- 01 November 1997, pp. 417-424
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Growth rates in terms of area expansion per 30 min were measured in the red alga Porphyra leucosticta under different light/dark (LD) cycles, irradiance levels and light qualities. Twelve hours per day under white light (35 μmol m−2 s−1) promoted a dramatic and rapid increase in thallus expansion during the first part of the light period followed by low values during the remaining light and dark phase. Light/dark regimes of 8[ratio ]8 h, 6[ratio ]6 h, 3[ratio ]3 h and 1·5[ratio ]1·5 h resulted in a discontinuous growth pattern where thallus expansion was restricted to the light phase while no growth occurred in the dark phase, and there was even a significant thallus contraction just after light-off. Growth rates in terms of percentage area increased with irradiance at LD 12[ratio ]12. This was due to: (1) the phase of high growth rate following the initial ‘morning peak’ extending from the first 6 h of the light phase to cover almost the entire light phase, and (2) an increase in growth rate during the second half of the night phase. Saturation was reached at an irradiance of 125 μmol m−2 s−1. An irradiance of 500 μmol m−2 s−1 decreased thallus expansion rate during the light and dark culture phases relative to the other irradiances used. Light quality also caused changes in growth rate: the maximum value was reached under yellow light followed by red; both of these were higher than the growth rate under white light. Blue light (35 μmol m−2 s−1) caused a decrease of more than 50% in thallus expansion compared with white or red light due to a very dramatic decrease in the ‘morning peak’ of thallus expansion and very low values in the rest of the light and dark phases. Increasing the percentage of blue light in different white light sources also decreased thallus expansion. It is suggested that light influences the growth of Porphyra in three ways: as an external signal matching thallus expansion with light and dark cycles; as an energy source promoting thallus expansion with increasing irradiance; and, at a morphogenetic level, inhibiting growth in blue light.