The effects of salinity on the cellular permeability and cytotoxicity of Heterosigma akashiwo

A laboratory study using the fish‐killing raphidophyte Heterosigma akashiwo was conducted to examine its capability to grow at salinities below oceanic, and to test the perceived relationship between reduced salinities and increased cytotoxicity. A nonaxenic strain of H. akashiwo isolated from the U.S. Pacific Northwest was exposed to a combination of three salinity (32, 20, and 10) and five temperature (14.7°C, 18.4°C, 21.4°C, 24.4°C and 27.8°C) conditions. Our results demonstrate that cell permeability and cytotoxicity are strongly correlated in unialgal cultures of H. akashiwo, which both increased as salinity decreased from 32 to 10. Furthermore, over a broad median range of salinities (10 and 20), neither temperature nor specific growth rate was correlated with cytotoxicity. However, in cultures grown at the salinity of 32, both temperature and specific growth rate were inversely proportional to toxicity; this relationship was likely due to the effect of contamination by an unidentified species of Skeletonema in those cultures. The presence of Skeletonema sp. resulted in a cytotoxic response from H. akashiwo that was greater than the response caused by salinity alone. These laboratory results reveal the capability of H. akashiwo to become more toxic not only at reduced salinities but also in competition with another algal species. Changes in cell permeability in response to salinity may be an acclimation mechanism by which H. akashiwo is able to respond rapidly to different salinities. Furthermore, due to its strong positive correlation with cytotoxicity, cellular permeability is potentially associated with the ichthyotoxic pathway of this raphytophyte.     

Broad Salinity Tolerance as a Refuge from Predation in the Harmful Raphidophyte Alga Heterosigma akashiwo (Raphidophyceae)

The ability of harmful algal species to form dense, nearly monospecific blooms remains an ecological and evolutionary puzzle. We hypothesized that predation interacts with estuarine salinity gradients to promote blooms of Heterosigma akashiwo (Y. Hada) Y. Hada ex Y. Hara et M. Chihara, a cosmopolitan toxic raphidophyte. Specifically, H. akashiwo's broad salinity tolerance appears to provide a refuge from predation that enhances the net growth of H. akashiwo populations through several mechanisms. (1) Contrasting salinity tolerance of predators and prey. Estuarine H. akashiwo isolates from the west coast of North America grew rapidly at salinities as low as six, and distributed throughout experimental salinity gradients to salinities as low as three. In contrast, survival of most protistan predator species was restricted to salinities >15. (2) H. akashiwo physiological and behavioral plasticity. Acclimation to low salinity enhanced H. akashiwo's ability to accumulate and grow in low salinity waters. In addition, the presence of a ciliate predator altered H. akashiwo swimming behavior, promoting accumulation in low‐salinity surface layers inhospitable to the ciliate. (3) Negative effects of low salinity on predation processes. Ciliate predation rates decreased sharply at salinities <25 and, for one species, H. akashiwo toxicity increased at low salinities. Taken together, these behaviors and responses imply that blooms can readily initiate in low salinity waters where H. akashiwo would experience decreased predation pressure while maintaining near‐maximal growth rates. The salinity structure of a typical estuary would provide this HAB species a unique refuge from predation. Broad salinity tolerance in raphidophytes may have evolved in part as a response to selective pressures associated with predation.     

Feeding by the heterotrophic dinoflagellate Oxyrrhis marina on the red-tide raphidophyte Heterosigma akashiwo: a potential biological method to control red tides using mass-cultured grazers

As part of the development of a method to control the outbreak and persistence of red tides using mass-cultured heterotrophic protist grazers, we measured the growth and ingestion rates of cultured Oxyrrhis marina (a heterotrophic dinoflagellate) on cultured Heterosigma akashiwo (a raphidophyte) in bottles in the laboratory and in mesocosms (ca. 60 liter) in nature, and those of the cultured grazer on natural populations of the red-tide organism in mesocosms set up in nature. In the bottle incubation, specific growth rates of O. marina increased rapidly with increasing concentration of cultured prey up to ca. 950 ng C ml(-1) (equivalent to 9,500 cells ml(-1)), but were saturated at higher concentrations. Maximum specific growth rate (mumax), KGR (prey concentration sustaining 0.5 mumax) and threshold prey concentration of O. marina on H. akashiwo were 1.43 d(-1), 104 ng C ml(-1), and 8.0 ng C ml(-1), respectively. Maximum ingestion and clearance rates of O. marina were 1.27 ng C grazer(-1) d(-1) and 0.3 microl grazer(-1) h(-1), respectively. Cultured O. marina grew well effectively reducing cultured and natural populations of H. akashiwo down to a very low concentration within 3 d in the mesocosms. The growth and ingestion rates of cultured O. marina on natural populations of H. akashiwo in the mesocosms were 39% and 40%, respectively, of those calculated based on the results from the bottle incubation in the laboratory, while growth and ingestion rates of cultured O. marina on cultured H. akashiwo in the mesocosms were 55% and 36%, respectively. Calculated grazing impact by O. marina on natural populations of H. akashiwo suggests that O. marina cultured on a large scale could be used for controlling red tides by H. akashiwo near aquaculture farms that are located in small ponds, lagoons, semi-enclosed bays, and large land-aqua tanks to which fresh seawater should be frequently supplied.     

Contrasting effects of high‐intensity photosynthetically active radiation on two bloom‐forming dinoflagellates

While light limitation can inhibit bloom formation in dinoflagellates, the potential for high‐intensity photosynthetically active radiation (PAR) to inhibit blooms by causing stress or damage has not been well‐studied. We measured the effects of high‐intensity PAR on the bloom‐forming dinoflagellates Alexandrium fundyense and Heterocapsa rotundata. Various physiological parameters (photosynthetic efficiency F_v/F_m, cell permeability, dimethylsulfoniopropionate [DMSP], cell volume, and chlorophyll‐a content) were measured before and after exposure to high‐intensity natural sunlight in short‐term light stress experiments. In addition, photosynthesis‐irradiance (P‐E) responses were compared for cells grown at different light levels to assess the capacity for photophysiological acclimation in each species. Experiments revealed distinct species‐specific responses to high PAR. While high light decreased F_v/F_m in both species, A. fundyense showed little additional evidence of light stress in short‐term experiments, although increased membrane permeability and intracellular DMSP indicated a response to handling. P‐E responses further indicated a high light‐adapted species with Chl‐a inversely proportional to growth irradiance and no evidence of photoinhibition; reduced maximum per‐cell photosynthesis rates suggest a trade‐off between photoprotection and C fixation in high light‐acclimated cells. Heterocapsa rotundata cells, in contrast, swelled in response to high light and sometimes lysed in short‐term experiments, releasing DMSP. P‐E responses confirmed a low light‐adapted species with high photosynthetic efficiencies associated with trade‐offs in the form of substantial photoinhibition and a lack of plasticity in Chl‐a content. These contrasting responses illustrate that high light constrains dinoflagellate community composition through species‐specific stress effects, with consequences for bloom formation and ecological interactions within the plankton.     

Morphological and genetic characterization of bloom‐forming Raphidophyceae from Brazilian coast

Massive fish kills caused by bloom‐forming species of the Raphidophyceae occur in many marine coastal areas and often cause significant economic losses. The ultrastructure and phylogeny of marine raphidophytes from the Brazilian coast have not been fully analyzed. Here, we present the first combined morphological and genetic characterization of raphidophyte strains from the Brazilian coast. Ten strains of four raphidophyte species (Chattonella subsalsa, C. antiqua, Heterosigma akashiwo, and Fibrocapsa japonica) were characterized based on morphology (including ultrastructure) and LSU rDNA sequences. Chattonella subsalsa and C. antiqua formed two distinct genetic clades. We found that the cell size is the only phenotypic feature separating C. subsalsa and C. antiqua strains from Brazil, whereas traditional characteristics used for species separation in the genus Chattonella (i.e., tail size, chloroplast presence in the tail, ‘oboe‐shaped’ mucocysts, and presence of thylakoids in the pyrenoid matrix) were not sufficiently discriminative, due to their overlapping in the two taxa. The phylogenetic analysis indicated intra‐specific geographic differences among C. subsalsa sequences, with two subclades: one formed by isolates from Brazil, USA, and Iran, and another by a sequence from the Adriatic Sea (Italy). Fibrocapsa japonica also showed intra‐specific geographic differences, with a sequence from a Brazilian strain grouped with strains from Japan, Australia, and Germany, all of them distinct from the Italian isolates. This is the first combined morphological and phylogenetic analysis of raphidophytes from the South Atlantic. Our findings broaden knowledge of the biodiversity of this important bloom‐forming algal group.     

The mechanism of competition between two bloom‐forming Microcystis species

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Viral attack exacerbates the susceptibility of a bloom‐forming alga to ocean acidification

Both ocean acidification and viral infection bring about changes in marine phytoplankton physiological activities and community composition. However, little information is available on how the relationship between phytoplankton and viruses may be affected by ocean acidification and what impacts this might have on photosynthesis‐driven marine biological CO₂ pump. Here, we show that when the harmful bloom alga Phaeocystis globosa is infected with viruses under future ocean conditions, its photosynthetic performance further decreased and cells became more susceptible to stressful light levels, showing enhanced photoinhibition and reduced carbon fixation, up‐regulation of mitochondrial respiration and decreased virus burst size. Our results indicate that ocean acidification exacerbates the impacts of viral attack on P. globosa, which implies that, while ocean acidification directly influences marine primary producers, it may also affect them indirectly by altering their relationship with viruses. Therefore, viruses as a biotic stressor need to be invoked when considering the overall impacts of climate change on marine productivity and carbon sequestration.     

Comparative mitochondrial genome analysis reveals the evolutionary rearrangement mechanism in Brassica

The genus Brassica has many species that are important for oil, vegetable and other food products. Three mitochondrial genome types (mitotype) originated from its common ancestor. In this paper, a B. nigra mitochondrial main circle genome with 232,407 bp was generated through de novo assembly. Synteny analysis showed that the mitochondrial genomes of B. rapa and B. oleracea had a better syntenic relationship than B. nigra. Principal components analysis and development of a phylogenetic tree indicated maternal ancestors of three allotetraploid species in Us triangle of Brassica. Diversified mitotypes were found in allotetraploid B. napus, in which napus‐type B. napus was derived from B. oleracea, while polima‐type B. napus was inherited from B. rapa. In addition, the mitochondrial genome of napus‐type B. napus was closer to botrytis‐type than capitata‐type B. oleracea. The sub‐stoichiometric shifting of several mitochondrial genes suggested that mitochondrial genome rearrangement underwent evolutionary selection during domestication and/or plant breeding. Our findings clarify the role of diploid species in the maternal origin of allotetraploid species in Brassica and suggest the possibility of breeding selection of the mitochondrial genome.     

Characterization of the first mitochondrial genome of a catenulid flatworm: Stenostomum leucops (Platyhelminthes)

The first complete mitochondrial genome of a catenulid, Stenostomum leucops, was characterized. Illumina sequencing and 90 813 reads were utilized in the assembly, producing one contig with an average coverage of 1118×. The length of this genome is 15 742 bp with 12 protein‐coding, two rRNA and 22 tRNA genes. Although the atp8 gene is absent in other Platyhelminthes, a highly divergent putative atp8 gene was found in S. leucops. In contrast to other Platyhelminthes, the mitochondrial genes of S. leucops are encoded on both strands. The gene order in the S. leucops mitogenome is very divergent from those observed in other Platyhelminthes, showing only small blocks of synteny. With AAA as the codon for lysine S. leucops shows the probable plesiomorphic condition, whereas Rhabditophora possess the derived GAA. This evolutionary transition is correlated with changes in the respective anticodons in trnK. It remains unclear whether the absence of the D arm and loop in trnS1 is a convergence in Catenulida and Neodermata.     

Complete mitochondrial genome sequence of the Himalayan Griffon,Gyps himalayensis (Accipitriformes: Accipitridae): Sequence,structure, and phylogenetic analyses

This is the first study to describe the mitochondrial genome of the Himalayan Griffon, Gyps himalayensis, which is an Old World vulture belonging to the family Accipitridae and occurring along the Himalayas and the adjoining Tibetan Plateau. Its mitogenome is a closed circular molecule 17,381 bp in size containing 13 protein‐coding genes, 22 tRNA coding genes, two rRNA‐coding genes, a control region (CR), and an extra pseudo‐control region (CCR) that are conserved in most Accipitridae mitogenomes. The overall base composition of the G. himalayensis mitogenome is 24.55% A, 29.49% T, 31.59% C, and 14.37% G, which is typical for bird mitochondrial genomes. The alignment of the Accipitridae species control regions showed high levels of genetic variation and abundant AT content. At the 5′ end of the domain I region, a long continuous poly‐C sequence was found. Two tandem repeats were found in the pseudo‐control regions. Phylogenetic analysis with Bayesian inference and maximum likelihood based on 13 protein‐coding genes indicated that the relationships at the family level were (Falconidae + (Cathartidae + (Sagittariidae + (Accipitridae + Pandionidae))). In the Accipitridae clade, G. himalayensis is more closely related to Aegypius monachus than to Spilornis cheela. The complete mitogenome of G. himalayensis provides a potentially useful resource for further exploration of the taxonomic status and phylogenetic history of Gyps species.     

Diurnal fluctuations in chloroplast GSH redox state regulate susceptibility to oxidative stress and cell fate in a bloom‐forming diatom

Diatoms are one of the key phytoplankton groups in the ocean, forming vast oceanic blooms and playing a significant part in global primary production. To shed light on the role of redox metabolism in diatom's acclimation to light–dark transition and its interplay with cell fate regulation, we generated transgenic lines of the diatom Thalassiosira pseudonana that express the redox‐sensitive green fluorescent protein targeted to various subcellular organelles. We detected organelle‐specific redox patterns in response to oxidative stress, indicating compartmentalized antioxidant capacities. Monitoring the GSH redox potential (E_GSH) in the chloroplast over diurnal cycles revealed distinct rhythmic patterns. Intriguingly, in the dark, cells exhibited reduced basal chloroplast E_GSH but higher sensitivity to oxidative stress than cells in the light. This dark‐dependent sensitivity to oxidative stress was a result of a depleted pool of reduced glutathione which accumulated during the light period. Interestingly, reduction in the chloroplast E_GSH was observed in the light phase prior to the transition to darkness, suggesting an anticipatory phase. Rapid chloroplast E_GSH re‐oxidation was observed upon re‐illumination, signifying an induction of an oxidative signaling during transition to light that may regulate downstream metabolic processes. Since light–dark transitions can dictate metabolic capabilities and susceptibility to a range of environmental stress conditions, deepening our understanding of the molecular components mediating the light‐dependent redox signals may provide novel insights into cell fate regulation and its impact on oceanic bloom successions.     

Effects of UVB Radiation on competition between the bloom‐forming cyanobacterium Microcystis aeruginosa and the Chlorophyceae Chlamydomonas microsphaera1

The growth, photosynthetic characteristics, and competitive ability of three algal strains were investigated under different doses of ultraviolet‐B (UVB) radiation (0, 0.285, and 0.372 W · m^?2). The organisms were the toxic bloom‐forming cyanobacterium Microcystis aeruginosa FACHB 912, nontoxic M. aeruginosa FACHB 469, and the green microalga Chlamydomonas microsphaera FACHB 52. In monocultures, the growth of all three strains was inhibited by UVB. In mixed cultures, enhanced UVB radiation resulted in decreased percentages of the two M. aeruginosa strains (19%–22% decrease on d 12 of the competition experiment). UVB radiation resulted in increased contents of chlorophyll a, b, and carotenoids (CAR) in C. microsphaera, and decreased contents of allophycocyanin (APC) or phycocyanin in the two Microcystis strains. All three strains showed increased levels of UVabsorbing compounds and intracellular reactive oxygen species under 0.372 W · m^?2 UVB radiation, and decreased light compensation points, dark respiratory rates, and maximal quantum efficiency of PSII. After a 20 h recovery, the photosynthetic oxygen evolution of C. microsphaera was restored to its maximum value, but that of Microcystis strains continued to decrease. Nonphotochemical quenching was increased by UVB radiation in C. microsphaera, but was unaffected in the two M. aeruginosa strains. Our results indicated that C. microsphaera has a competitive advantage relative to Microcystis during exposure to UVB irradiation.     

Glacial refuges for three‐spined stickleback in the Iberian Peninsula: mitochondrial DNA phylogeography

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Phylogeography of the freshwater raphidophyte Gonyostomum semen confirms a recent expansion in northern Europe by a single haplotype

Gonyostmum semen is a freshwater raphidophyte that has increased in occurrence and abundance in several countries in northern Europe since the 1980s. More recently, the species has expanded rapidly also in north‐eastern Europe, and it is frequently referred to as invasive. To better understand the species history, we have explored the phylogeography of G. semen using strains from northern Europe, United States, and Japan. Three regions of the ribosomal RNA gene (small subunit [SSU], internal transcribed spacer [ITS] and large subunit [LSU]) and one mitochondrial DNA marker (cox1) were analyzed. The SSU and partial LSU sequences were identical in all strains, confirming that they belong to the same species. The ITS region differentiated the American from the other strains, but showed high intra‐strain variability. In contrast, the mitochondrial marker cox1 showed distinct differences between the European, American, and Japanese strains. Interestingly, only one cox1 haplotype was detected in European strains. The overall low diversity and weak geographic structure within northern European strains supported the hypothesis of a recent invasion of new lakes by G. semen. Our data also show that the invasive northern European lineage is genetically distinct from the lineages from the other continents. Finally, we concluded that the mitochondrial cox1 was the most useful marker in determining large‐scale biogeographic patterns in this species.     

Discovery of a resting stage in the harmful,brown‐tide‐causing pelagophyte,Aureoumbra lagunensis: a mechanism potentially facilitating recurrent blooms and geographic expansion

To date, the life stages of pelagophytes have been poorly described. This study describes the ability of Aureoumbra lagunensis to enter a resting stage in response to environmental stressors including high temperature, nutrient depletion, and darkness as well as their ability to revert from resting cells back to vegetative cells after exposure to optimal light, temperature, and nutrient conditions. Resting cells became round in shape and larger in size, filled with red accumulation bodies, had smaller and fewer plastids, more vacuolar space, contained lower concentrations of chl a and RNA, displayed reduced photosynthetic efficiency, and lower respiration rates relative to vegetative cells. Analysis of vegetative and resting cells using Raman microspectrometry indicated resting cells were enriched in sterols within red accumulation bodies and were depleted in pigments relative to vegetative cells. Upon reverting to vegetative cells, cells increased their chl a content, photosynthetic efficiency, respiration rate, and growth rate and lost accumulation bodies as they became smaller. The time required for resting cells to resume vegetative growth was proportional to both the duration and temperature of dark storage, possibly due to higher metabolic demands on stored energy (sterols) reserves during longer period of storage and/or storage at higher temperature (20°C vs. 10°C). Resting cells kept in the dark at 10°C for 7 months readily reverted back to vegetative cells when transferred to optimal conditions. Thus, the ability of Aureoumbra to form a resting stage likely enables them to form annual blooms within subtropic ecosystems, resist temperature extremes, and may facilitate geographic expansion via anthropogenic transport.     

Sequence capture and next‐generation sequencing of ultraconserved elements in a large‐genome salamander

Amidst the rapid advancement in next‐generation sequencing (NGS) technology over the last few years, salamanders have been left behind. Salamanders have enormous genomes—up to 40 times the size of the human genome—and this poses challenges to generating NGS data sets of quality and quantity similar to those of other vertebrates. However, optimization of laboratory protocols is time‐consuming and often cost prohibitive, and continued omission of salamanders from novel phylogeographic research is detrimental to species facing decline. Here, we use a salamander endemic to the southeastern United States, Plethodon serratus, to test the utility of an established protocol for sequence capture of ultraconserved elements (UCEs) in resolving intraspecific phylogeographic relationships and delimiting cryptic species. Without modifying the standard laboratory protocol, we generated a data set consisting of over 600 million reads for 85 P. serratus samples. Species delimitation analyses support recognition of seven species within P. serratus sensu lato, and all phylogenetic relationships among the seven species are fully resolved under a coalescent model. Results also corroborate previous data suggesting nonmonophyly of the Ouachita and Louisiana regions. Our results demonstrate that established UCE protocols can successfully be used in phylogeographic studies of salamander species, providing a powerful tool for future research on evolutionary history of amphibians and other organisms with large genomes.     

The effects of allospecific mitochondrial genome on the fitness of northern redbelly dace (Chrosomus eos)

Instantaneous mitochondrial introgression events allow the disentangling of the effects of hybridization from those of allospecific mtDNA. Such process frequently occurred in the fish Chrosomus eos, resulting in cybrid individuals composed of a C. eos nuclear genome but with a C. neogaeus mtDNA. This provides a valuable model to address the fundamental question: How well do introgressed individuals perform in their native environment? We infer where de novo production of cybrids occurred to discriminate native environments from those colonized by cybrids in 25 sites from two regions (West‐Qc and East‐Qc) in Quebec (Canada). We then compared the relative abundance of wild types and cybrids as a measure integrating both fitness and de novo production of cybrids. According to mtDNA variation, 12 introgression events are required to explain the diversity of cybrids. Five cybrid lineages could not be associated with in situ introgression events. This includes one haplotype carried by 93% of the cybrids expected to have colonized West‐Qc. These cybrids also displayed a nearly complete allopatric distribution with wild types. We still inferred de novo production of cybrids at seven sites, that accounted for 70% of the cybrids in East‐Qc. Wild‐type and cybrid individuals coexist in all East‐Qc sites while cybrids were less abundant. Allopatry of cybrids restricted to the postglacial expansion suggests the existence of higher fitness for cybrids in specific conditions, allowing for the colonization of different environments and expanding the species’ range. However, allospecific mtDNA does not provide a higher fitness to cybrids in their native environment compared to wild types, making the success of an introgressed lineage uncertain.     

Effects of iron deficiency on the growth and photosynthesis of three bloom‐forming cyanobacterial species isolated from Lake Taihu

Cyanobacterial blooms are found in many freshwater ecosystems around the world, but the effect of environmental factors on their growth and the proportion of species still require more investigation. In this study, the physiological responses of bloom‐forming cyanobacteria M icrocystis aeruginosa FACHB912, M icrocystis flos‐aquae FACHB1028 and P seudanabaena sp. FACHB1282 to iron deficiency were investigated. Their specific growth rates were found to decrease as the available iron concentration decreased. At low available iron concentrations of 1 × 10^?7 M (pFe 21.3) and 5 × 10^?8 M (pFe 21.6), M . aeruginosa had the lowest specific growth rate among three studied species. The cell sizes of M . flos‐aquae and Pseudanabaena sp. were significantly smaller under the lowest iron concentration. The chlorophyll a content of the three species decreased at the lowest iron concentration. The maximal relative electron transport rate, photosynthetic efficiency, and light‐saturation parameter of M . aeruginosa were lower than the other two cyanobacteria at pFe 21.3. Therefore, M . aeruginosa was the least able to adapt to iron deficiency. Under iron deficiency, the functional absorption cross‐section of PSII and electron transport rate on the acceptor side of PSII decreased in M . aeruginosa, while the connectivity factor between individual photosynthetic units increased in M . flos‐aquae, and the electron transport rate on the acceptor side of PSII and between PSII and PSI decreased in P seudanabaena sp. The ability to store iron was highest in M . flos‐aquae, followed by P seudanabaena sp. and M . aeruginosa. Thus, these results provide necessary information for detecting the role of iron in the succession of cyanobacterial species in Lake Taihu, the third largest freshwater lake in China, because all three species were isolated from this lake.