An investigation of non-steady-state algal growth. II. Mathematical modelling of co-nutrient-limited algal growth

The ability of mathematical models to simulate competition for nutrients between three algal species, the diatom Thalassiosira pseudonana, a marine raphidophyte Heterosigma carterae and the dinoflagellate Alexandrium minutum, was investigated. Transient growth models were parameterized and tested using a number of closely controlled laboratory data sets including batch monocultures, batch competition experiments and semi-continuous culture competition experiments. The cell quota model of algal growth was found to be adequate to simulate growth of both the raphidophyte and the dinoflagellate. Batch monoculture data for diatom growth obtained under either nitrogen (N) or silicon (Si) limitation could also be simulated with a quota-style model, which in this case included feedback inhibition of nutrient uptake. However, to simulate both batch and semi-continuous culture experiments (and competition between the species), it was necessary to consider diatom Si-N metabolism. A model was derived which contains a representation of both intracellular N ad Si, and of the interaction of these nutrients within the cell. The model used a co-nutrient limitation based on the perceived functional and structural role of N and Si, respectively, within the cell. Simulations indicated that models capable of adequately representing monoculture growth in batch culture may produce erroneous results when incorporated into models of competition. The co-nutrient model is a first step to producing tractable algal growth models which will represent multiple nutrient stress in transient growth conditions.      

Ottia meiospora (Ottiaceae,Rhodophyta), a new genus and family endophytic within the thallus of Nothocladus (Batrachospermales,Rhodophyta)

A new genus, Ottia, and family, Ottiaceae, are proposed within the Acrochaetiales to accommodate the uniseriate red algal endophyte of batrachspermalean taxa previously named Balbiania meiospora. Prior to this study, Balbiania investiens was transferred to its own family and order (Balbianiales) based on comparative DNA sequence data and a distinctive reproductive morphology. However, the second species described in this genus, B. meiospora, continued to be treated as a species of Audouinella (A. meiospora) pending further investigation. Phylogenetic analyses of sequence data confirmed only a distant relationship between the two endophytes, and a closer alliance of B. meiospora to Acrochaetiales. The data also showed that Ottia meiospora was the deepest diverging lineage in the Acrochaetiales, sister to all of the currently recognized genera and families. In this study, we review the classification of what we now call O. meiospora – reported from Australia, New Zealand and Brazil – based on sequence and morphological data. Morphological observations provided little clarity around the reproductive morphology or the life cycle of this endophyte of Nothocladus s. lat. found commonly in mainland Australia but, to date, less so in New Zealand.     

The complete chloroplast genome of Gracilariopsis lemaneiformis (Rhodophyta) gives new insight into the evolution of family Gracilariaceae

The complete chloroplast genome of Gracilariopsis lemaneiformis was recovered from a Next Generation Sequencing data set. Without quadripartite structure, this chloroplast genome (183,013 bp, 27.40% GC content) contains 202 protein‐coding genes, 34 tRNA genes, 3 rRNA genes, and 1 tmRNA gene. Synteny analysis showed plasmid incorporation regions in chloroplast genomes of three species of family Gracilariaceae and in Grateloupia taiwanensis of family Halymeniaceae. Combined with reported red algal plasmid sequences in nuclear and mitochondrial genomes, we postulated that red algal plasmids may have played an important role in ancient horizontal gene transfer among nuclear, chloroplast, and mitochondrial genomes. Substitution rate analysis showed that purifying selective forces maintaining stability of protein‐coding genes of nine red algal chloroplast genomes over long periods must be strong and that the forces acting on gene groups and single genes of nine red algal chloroplast genomes were similar and consistent. The divergence of Gp. lemaneiformis occurred ~447.98 million years ago (Mya), close to the divergence time of genus Pyropia and Porphyra (443.62 Mya).     

Interaction mechanisms between Gracilaria chilensis (Rhodophyta) and epiphytes

Epiphytes can have a considerable effect on Gracilaria production, and Ulva is one of the commonest algal species identified as an epiphyte, reaching loads of 60% (g of epiphytes per g of Gracilaria) in the intertidal cultures of southern Chile. This study evaluates the relative importance of light reduction, addition of weight to the host thalli and nutrient depletion, as mechanisms determining the interaction effects of Ulva epiphytes on Gracilaria cultivation. Using field experiments undertaken during the main Gracilaria growth season (spring), we evaluate the mechanisms of epiphyte-host algae interaction by manipulating artificial epiphytes. The results indicate that Ulva can significantly depress Gracilaria biomass production and that the addition of weight to the host algae and the consequent dislodgement increase, appear to be the main mechanisms involved in the Ulva-Gracilaria interaction. However, the light reduction caused by the epiphytes can also partially explain the reduction in Gracilaria production. Nutrients depletion would not appear to fully account for the detrimental effects of Ulva over Gracilaria in intertidal farming areas of southern Chile.     

Characterization of an agar fraction extracted from Gracilaria dura (Gracilariales,Rhodophyta)

The evaluation of biopolymers of biotechnological interest has stressed the importance of renewable sources from the northern Adriatic Sea. In the frame of this research program, the red alga Gracilaria cf. dura, has been studied. Agar was obtained from Gracilaria cf. dura by means of alkali treatment and hot water extraction. In order to purify the extracts, amylase and isopropyl alcohol were used. Analysis of sugars was carried out by means of gas chromatography on alditol acetate derivatives; sulfate content was evaluated by means of infrared spectroscopy. An analysis of molecular weight distribution was carried out by means of high performance gel permeation chromatography coupled with a low angle laser light scattering device as detector. Analytical data were examined in terms of specificity of the algal source utilized, and the agar fractions extracted by means of this procedure were compared with a commercial sample.     

Growth interactions among blue-green (Anabaena Oscillarioides,Microcystis aeruginosa) and green (Chlorella sp.) algae

The growth interactions amongst the blue-green algal species Anabaena oscillarioides, Microcystis aeruginosa and the green alga, Chlorella sp. were studied both in mixed cultures and in filter cultures separated by a membrane filter in the two arms of an interaction U-tube. The role of nutrients especially phosphate upon the interaction has also been studied. Anabaena and Microcystis both inhibited the growth of Chlorella while Microcystis also inhibited the growth of Anabaena. The inhibitory effect of Microcystis was found to be dependent on high concentrations of the initial algal inocula and independent of the initial concentration of nutrients such as inorganic phosphate, indicating that the nature of the inhibition is probably due to the production of inhibitory extracellular products by Microcystis. On the other hand, the inhibitory effect of Anabaena on Chlorella is the consequence of nutrient competition with Anabaena competing more effectively for the available phosphate.     

A discrete-time logistic model of frond dynamics for Mazzaella parksii (Rhodophyta, Gigartinales)

Mathematical modelling is useful in population ecology and resource management. Logistic models have traditionally been applied to unitary organisms, but it is unclear whether they could be used at the frond (ramet) level for clonal seaweeds. This study shows that frond dynamics for the clonal seaweed Mazzaella parksii (=M. cornucopiae) can be described by a discrete-time logistic model. The model is realistic in that it includes density-dependence, which was previously demonstrated experimentally for this species, and only necessitates data on frond density measured at discrete time intervals. This may constitute a useful tool for the management of clonal seaweeds of economic importance that occur in dense stands. This revised version was published online in August 2006 with corrections to the Cover Date.     

Responses to ocean acidification and diurnal temperature variation in a commercially farmed seaweed,Pyropia haitanensis (Rhodophyta)

To investigate carbon and nitrogen metabolism in Pyropia haitanensis in response to the combined conditions of ocean acidification and diurnal temperature variation, maricultured thalli were tested in acidified culture under different temperature treatments. The results showed a combined effect of ocean acidification and diurnal temperature difference on the C and N metabolism and growth of P. haitanensis. In acidifed culture, algal growth, maximum photosynthetic rate, nitrate reductase (NR) activity, amino acid (AA) content and AA score (AAS) were more significantly enhanced in seaweed under diurnal temperature variation than in seaweed at constant temperature. In acidified seawater, soluble carbohydrates in P. haitanensis increased due to greater dissolved inorganic carbon (DIC), whereas soluble proteins decreased. Under the diurnal temperature treatment, higher temperature during the light period enhanced accumulation of algal photosynthates, whereas lower temperature in the dark period reduced energy consumption, resulting in enhanced algal growth, AA content and AAS. We concluded that suitable diurnal temperature difference would be conducive to C fixation and N assimilation under ocean acidification. However, excessively high temperatures would depress algal photosynthesis and increase energy consumption, thereby exerting a negative effect on algal growth.     

Comparative physiological studies on the growth of cryptic species of Bostrychia intricata (Rhodomelaceae,Rhodophyta) in various salinity and temperature conditions

Inter‐ and intra‐specific physiological variations of intertidal macroalgae have been well investigated. However, studies on physiological responses of cryptic algal species have been poorly documented. Bostrychia intricata is a widespread marine red alga in the Southern Hemisphere, and has many cryptic species. We investigated the effect of different salinities and temperatures on the specific growth rate of three cryptic species (N2, N4 and N5) of B. intricata from New Zealand. Our data indicated that all cryptic species grew at the full range of salinities and temperatures tested, but exhibited a significant difference in their specific growth rates. Cryptic species N4 had a higher growth rate than the other two cryptic species under all experimental conditions, whereas cryptic species N2 occasionally showed a higher growth rate than cryptic species N5 at high salinities and lower temperatures. The distinct physiological properties of these cryptic species may explain their distribution pattern (a wider distribution of cryptic species N4 than N2 and N5) in New Zealand. The physiological divergence between the cryptic species could be related to their levels of evolutionary divergence, with more similar physiology between cryptic species, which share a more recent common ancestor (N2 and N5). Our findings underline that morphologically indistinguishable cryptic algal species are different in many other aspects and are truly independent entities.     

Competition between the photosynthetic and the (chloro)respiratory electron transport chains in cyanobacteria, green algae and higher plants. Effect of heat stress

By measuring the effect of cyanide on the flash-induced redox reactions of the cytochrome (cyt) b ₆/f complex we carried out a comparative study in order to characterize the interaction between the photosynthetic and the respiratory electron transport systems in cyanobacterial (Synechococcus sp. PCC 6301) and green algal (Chlamydomonas reinhardtii) cells, and in tobacco (Nicotiana tabacum L. cv. Petit Havana SR1) protoplasts. We found that the addition of 1 mM KCN resulted in a significant acceleration of the rereduction-rate of cyt f ⁺. This enhancement of the activity of the cyt b ₆/f complex apparently occurred with the same mechanism in prokaryotes and eukaryotes, and its dependence on the concentration of KCN in eukaryotes ruled out an origin in mitorespiration, superoxide dismutase and plastocyanin, strongly suggesting that a cyanide-sensitive terminal oxidase, a putative component of chlororespiration, competes with photosystem 1 (PS1) for electrons from the plastoquionone (PQ) pool. Concerning the physiological role of the competition between the (chloro)respiratory and the photosynthetic electron transport systems, our data obtained with cyanobacterial and algal cells incubated at elevated temperatures (30–50 °C) showed that the respiratory control over photosynthesis became significant in cells exposed to heat-stress. This revised version was published online in August 2006 with corrections to the Cover Date.     

Reassessment of the taxonomic status of Gelidium subfastigiatum (Gelidiales, Rhodophyta)

The taxonomic relationship between Gelidium elegans Kützing and Gelidium subfastigiatum Okamura, two morphologically similar species of the red algal genus Gelidium (Gelidiaceae) growing in the north‐western Pacific, was critically re‐examined. Gelidium subfastigiatum has been distinguished from G. elegans by its more robust thalli, which have antrorse tooth‐like branches, although their distinction has been said to be often difficult or impossible. We determined the nuclear encoded internal transcribed spacer 1 (ITS1) for 14 samples from eight populations of this G. elegans/ G. subfastigiatum complex, and two types of ITS1 sequences were found. Analysis of seasonal variations of subterminal portions of major branches revealed that this complex includes two groups: one possessing the type 1 ITS1 sequence and antrorse tooth‐like branches that are subterminally thickened and widened during only colder months, and another possessing the type 2 ITS1 sequence and thin and narrow branches throughout the year. These groups should be recognized as separate species; the former is assigned to G. subfastigiatum and the latter to G. elegans.     

Genetic and morphological variation in an ecosystem engineer,Lithophyllum byssoides (Corallinales,Rhodophyta)

Lithophyllum byssoides is a common coralline alga in the intertidal zone of Mediterranean coasts, where it produces biogenic concretions housing a high algal and invertebrate biodiversity. This species is an ecosystem engineer and is considered a target for conservation efforts, but designing effective conservation strategies currently is impossible due to lack of information about its population structure. The morphological and molecular variation of L. byssoides was investigated using morphoanatomy and DNA sequences (psbA and cox2,3) obtained from populations at 15 localities on the Italian and Croatian coasts. Lithophyllum byssoides exhibited a high number of haplotypes (31 psbA haplotypes and 24 cox2,3 haplotypes) in the central Mediterranean. The psbA and cox2,3 phylogenies were congruent and showed seven lineages. For most of these clades, the distribution was limited to one or a few localities, but one of them (clade 7) was widespread across the central Mediterranean, spanning the main biogeographic boundaries recognized in this area. The central Mediterranean populations formed a lineage separate from Atlantic samples; psbA pair‐wise divergences suggested that recognition of Atlantic and Mediterranean L. byssoides as different species may be appropriate. The central Mediterranean haplotype patterns of L. byssoides were interpreted as resulting from past climatic events in the hydrogeological history of the Mediterranean Sea. The high haplotype diversity and the restricted spatial distribution of the seven lineages suggest that individual populations should be managed as independent units.     

Taxonomic and biostratigraphical re-assessments of Subterraniphyllum Elliott (Corallinales, Rhodophyta)

A taxonomic and biostratigraphical re‐assessment of Subterraniphyllum Elliott (Corallinales, Rhodophyta) is presented. Results from studies of the type collection and of newly collected material from north‐eastern Italy and northern Slovenia have shown that this taxon is not a geniculate coralline red alga as originally suggested by Elliott and most subsequent authors. Vegetatively, Subterraniphyllum most closely resembles certain living members of the Corallinales; however, the phenetic and phylogenetic relationships of Subterraniphyllum to other Corallinales cannot be determined with greater certainty. The exclusion of Subterraniphyllum from any group of Corallinaceae with genicula is based on unequivocal evidence that branch formation does not involve the occurrence of genicula. Subterraniphyllum seems to be restricted to the Oligocene. Reports of occurrences in Upper Eocene and Lower Miocene sediments cannot be substantiated. Subterraniphyllum, however, cannot be considered a useful stratigraphical marker until further data on its occurrence in well‐dated carbonate sequences are acquired. This study illustrates the problems associated with placing fossil coralline algal specimens into geniculate genera without the preservation of relevant morphological characters. This is especially true in the absence of the careful assessment of fossil material with respect to current taxonomic concepts of geniculate coralline genera, all of which are based on studies of living species. According to the current concepts for geniculate coralline genera, the placing of fossil specimens into geniculate genera without appropriate evidence must be avoided by grouping all potentially geniculate fragments under the informal group ‘Geniculate sensu lato’. Furthermore, for all those many fossil specimens where unequivocal evidence is not present, it is possible to utilize ‘form genera’ based on characters that are normally preserved. This leads to creating a consistent, workable system of applying names to most fossil corallines so that they can be reliably used in relation to stratigraphical and palaeoecological studies.     

Multigene analyses resolve early diverging lineages in the Rhodymeniophycidae (Florideophyceae,Rhodophyta)

Multigene phylogenetic analyses were directed at resolving the earliest divergences in the red algal subclass Rhodymeniophycidae. The inclusion of key taxa (new to science and/or previously lacking molecular data), additional sequence data (SSU, LSU, EF2, rbcL, COI‐5P), and phylogenetic analyses removing the most variable sites (site stripping) have provided resolution for the first time at these deep nodes. The earliest diverging lineage within the subclass was the enigmatic Catenellopsis oligarthra from New Zealand (Catenellopsidaceae), which is here placed in the Catenellopsidales ord. nov. In our analyses, Atractophora hypnoides was not allied with the other included Bonnemaisoniales, but resolved as sister to the Peyssonneliales, and is here assigned to Atractophoraceae fam. nov. in the Atractophorales ord. nov. Inclusion of Acrothesaurum gemellifilum gen. et sp. nov. from Tasmania has greatly improved our understanding of the Acrosymphytales, to which we assign three families, the Acrosymphytaceae, Acrothesauraceae fam. nov. and Schimmelmanniaceae fam. nov.     

Bioremediation of nitrogenous compounds from oilfield wastewater by Ulva lactuca (Chlorophyta)

Oilfield wastewater (OFW) is a by-product of petroleum production and has a high nitrogen concentration. Bioremediation by macroalgae appears to be an option for OFW, and the genus Ulva (Chlorophyta) has strong potential as an agent of bioremediation because of its high nitrogen absorption capacity. This experimental study evaluated the efficiency of bioremediation of nitrogenous compounds in three concentrations of OFW by Ulva lactuca. One-phase decay models, photosynthetic status (assessed by pulse amplitude–modulated [PAM] fluorometry), and growth rate were used to assess bioremediation efficiency and algal physiology. All nitrogenous compounds were removed during the experimental period. The models that were applied for ammonium showed a stronger bioremediation effect for OFW at a concentration of 25% than at concentrations of 12.5% and 2.5%, and for nitrate, the models showed a stronger bioremediation effect at the 12.5% OFW concentration. The minor effects of OFW on photosynthetic performance and growth, added to high removal of nitrogen, emphasize the bioremediation capacity of U. lactuca, suggesting a new possibility of bioremediation of this waste.     

Phylogeography of the freshwater red alga Sirodotia (Batrachospermales,Rhodophyta) in Brazil

Considering the lack of knowledge on genetic variation on members of the freshwater red algal of the order Batrachospermales in tropical regions, phylogeographic patterns in Sirodotia populations were investigated using two mitochondrial regions: the cox2‐3 spacer and partial cox1 gene (barcode). Individuals identified as Sirodotia delicatula were analyzed from 14 stream segments across its distribution in Brazil. Phylogenetic analyses based on the ribulose‐1,5‐bisphosphate carboxylase/oxygenase large sub‐unit gene showed three clades, one representing S. delicatula, from all locations in southeastern Brazil and other regions from Brazil. The remaining samples formed two clades, which were highly divergent and distantly positioned from those of S. delicatula: 2.5–2.7% and 3.4–3.7%. This level of variation would warrant the species split of these taxa from mid‐western Brazil. A total of eight cox2‐3 spacer and nine cox1 haplotypes were observed among the 122 individuals studied. One location had two cox2‐3 haplotypes and three locations had two cox1 haplotypes; all others had a single dominant haplotype each. The existence of high intraspecific genetic variation among individuals of distinct locations (several haplotypes), but little variation within a location seems to be a pattern for the Batrachospermales. Haplotype networks showed low variation among the haplotypes from southeastern Brazil (10 locations with divergence of 0.3–1.1% for cox2‐3, 0.1–0.3% for cox1) and high variation among the haplotypes from the mid‐west region (four locations, 4.0–9.3% for cox2‐3, 6.2–8.4% for cox1). Thus, the present data clearly suggest the existence of cryptic species in Sirodotia in Brazil.     

Vegetative propagation and spore-based recruitment in the carrageenophyte Chondracanthus chamissoi (Gigartinales, Rhodophyta) in northern Chile

In the present study we compared vegetative and spore‐based propagation for Chondracanthus chamissoi (C. Agardh) Kützing. Monthly field observations were made over a 1‐year period at Puerto Aldea, Tongoy Bay, Chile. Data were collected both outside and within a bed of C. chamissoi. Vegetative propagation was assessed via attachment of drifting fronds to shell‐encrusted concrete blocks at both sites. Germination of spores was recorded on the same shell substrates. Substrate re‐adhesion varied seasonally between sectors. Highest averages occurred within the algal bed between January 1997 and March 1997. The number of sporelings showed two peaks of maximal recruitment in spring and summer months (January‐March 1997 and September 1997‐January 1998). Spore‐based propagation is an important mechanism of seasonal regeneration of biomass in the C. chamissoi bed; however, re‐attachment of fronds may have been important in maintaining production of the bed during the period of maximum biomass accumulation.     

Australian Laurencia majuscula (Rhodophyta,Rhodomelaceae) and the Brazilian Laurencia dendroidea are conspecific

Morphological and molecular studies have been undertaken on two species of the red algal genus Laurencia J.V.Lamouroux: Laurencia majuscula (Harvey) A.H.S. Lucas and Laurencia dendroidea J.Agardh, both from their type localities. The phylogenetic position of these species was inferred by analysis of the chloroplast‐encoded rbcL gene sequences from 24 taxa. In all phylogenetic analyses, the Australian Laurencia majuscula and the Brazilian L. dendroidea formed a well‐supported monophyletic clade within the Laurencia sensu stricto. This clade was divided into two subclades corresponding to each geographical region; however, the genetic divergence between Australian L. majuscula and Brazilian L. dendroidea was only 0–1.35%. Examination of the type specimens and sequences of freshly collected samples of both Laurencia majuscula and L. dendroidea show the two to be conspecific despite their disjunct type localities.