Evolution in temperature-dependent phytoplankton traits revealed from a sediment archive: do reaction norms tell the whole story?
ABSTRACT: The high evolutionary potential of phytoplankton species allows them to rapidly adapt to global warming. Adaptations may occur in temperature-dependent traits, such as growth rate, cell size and life cycle processes. Using resurrection experiments with resting stages from living sediment archives, it is possible to investigate whether adaptation occurred. For this study, we revived resting cysts of the spring bloom dinoflagellate Apocalathium malmogiense from recent and 100-year-old sediment layers from the Gulf of Finland, and compared temperature-dependent traits of recent and historic strains along a temperature gradient. We detected no changes in growth rates and cell sizes but a significant difference between recent and historic strains regarding resting cyst formation. The encystment rate of recent strains was significantly lower compared with historic strains which we interpret as an indication of adaptation to higher and more rapidly increasing spring temperatures. Low encystment rates may allow for bloom formation even if the threshold temperature inducing a loss of actively growing cells through resting cyst formation is exceeded. Our findings reveal that phenotypic responses of phytoplankton to changing temperature conditions may include hidden traits such as life cycle processes and their regulation mechanisms. This study emphasizes the potential of living sediment archives to investigate plankton responses and adaptation to global warming.
Project description:In seasonal environments, strong gradients of environmental parameters can shape life cycles of phytoplankton. Depending on the rate of environmental fluctuation, specialist or generalist strategies may be favored, potentially affecting life cycle transitions. The present study examined life cycle transitions of the toxin producing Baltic dinoflagellate Alexandrium ostenfeldii and their regulation by environmental factors (temperature and nutrients). This investigation aimed to determine whether genetic recombination of different strains is required for resting cyst formation and whether newly formed cysts are dormant. Field data (temperature and salinity) and sediment surface samples were collected from a site with recurrent blooms and germination and encystment experiments were conducted under controlled laboratory conditions. Results indicate a lack of seasonal germination pattern, set by an endogenous rhythm, as commonly found with other dinoflagellates from the Baltic Sea. Germination of quiescent cysts was triggered by temperatures exceeding 10°C and combined nutrient limitation of nitrogen and phosphorus or a drop in temperature from 16 to 10°C triggered encystment most efficiently. Genetic recombination was not mandatory for the formation of resting cysts, but supported higher numbers of resistant cysts and enhanced germination capacity after a resting period. Findings from this study confirm that A. ostenfeldii follows a generalist germination and cyst formation strategy, driven by strong seasonality, which may support its persistence and possibly expansion in marginal environments in the future, if higher temperatures facilitate a longer growth season.
Project description:Environmental conditions regulate the germination of phytoplankton resting stages. While some factors lead to synchronous germination, others stimulate germination of only a small fraction of the resting stages. This suggests that habitat filters may act on the germination level and thus affect selection of blooming strains. Benthic "seed banks" of the toxic dinoflagellate Alexandrium ostenfeldii from the Baltic Sea are genetically and phenotypically diverse, indicating a high potential for adaptation by selection on standing genetic variation. Here, we experimentally tested the role of climate-related salinity and temperature as selection filters during germination and subsequent establishment of A. ostenfeldii strains. A representative resting cyst population was isolated from sediment samples, and germination and reciprocal transplantation experiments were carried out, including four treatments: Average present day germination conditions and three potential future conditions: high temperature, low salinity, and high temperature in combination with low salinity. We found that the final germination success of A. ostenfeldii resting cysts was unaffected by temperature and salinity in the range tested. A high germination success of more than 80% in all treatments indicates that strains are not selected by temperature and salinity during germination, but selection becomes more important shortly after germination, in the vegetative stage of the life cycle. Moreover, strains were not adapted to germination conditions. Instead, highly plastic responses occurred after transplantation and significantly higher growth rates were observed at higher temperature. High variability of strain-specific responses has probably masked the overall effect of the treatments, highlighting the importance of testing the effect of environmental factors on many strains. It is likely that A. ostenfeldii populations can persist in the future, because suitable strains, which are able to germinate and grow well at potential future climate conditions, are part of the highly diverse cyst population. OPEN RESEARCH BADGES:This article has earned an Open Data Badge for making publicly available the digitally-shareable data necessary to reproduce the reported results. The data is available at https://doi.org/10.5061/dryad.c8c83nr.
Project description:Zooplankton blooms are a frequent phenomenon in tropical systems. However, drivers of bloom formation and the contribution of emerging resting eggs are largely unexplored. We investigated the dynamics and the triggers of rotifer blooms in African soda-lakes and assessed their impact on other trophic levels. A meta-analysis of rotifer peak densities including abundances of up to 6 × 10(5) individuals L(-1) demonstrated that rotifer bloom formation was uncoupled from the food environment and the seasonality of climatic conditions. A time series with weekly sampling intervals from Lake Nakuru (Kenya) revealed that intrinsic growth factors (food quality and the physicochemical environment) significantly affected rotifer population fluctuations, but were of minor importance for bloom formation. Instead, rotifer bloom formation was linked to sediment resuspension, a prerequisite for hatching of resting-eggs. Population growth rates exceed pelagic birth rates and simulations of rotifer dynamics confirmed the quantitative importance of rotifer emergence from the sediment egg-bank and signifying a decoupling of bloom formation from pelagic reproduction. Rotifer blooms led to a top-down control of small-sized algae and facilitated a switch to more grazing-resistant, filamentous cyanobacteria. This shift in phytoplankton composition cascaded up the food chain and triggered the return of filter-feeding flamingos. Calculations of consequent changes in the lake's energy budget and export of aquatic primary production to terrestrial ecosystems demonstrated the large potential impact of nonseasonal disturbances on the functioning of shallow tropical lakes.
Project description:Experimental evolution can be used to test for and characterize parasite and pathogen adaptation. We undertook a serial-passage experiment in which a single parasite population of the obligate fungal (chytrid) parasite Rhizophydium megarrhizum was maintained over a period of 200 days under different mono- and multiclonal compositions of its phytoplankton host, the bloom-forming cyanobacterium Planktothrix. Despite initially inferior performance, parasite populations under sustained exposure to novel monoclonal hosts experienced rapid fitness increases evidenced by increased transmission rates. This demonstrates rapid adaptation of chytrids to novel hosts and highlights their high evolutionary potential. In contrast, increased fitness was not detected in parasites exposed to multiclonal host mixtures, indicating that cyanobacterial intraspecific diversity hampers parasites adaptation. Significant increases in intensity of infection were observed in monoclonal and multiclonal treatments, suggesting high evolvability of traits involved in parasite attachment onto hosts (i.e., encystment). A comparison of the performance of evolved and unevolved (control) parasite populations against their common ancestral host did not reveal parasite attenuation. Our results exemplify the ability of chytrid parasites to adapt rapidly to new hosts, while providing experimental evidence that genetic diversity in host populations grants increased resistance to disease by hindering parasite adaptation.
Project description:Three diel field campaigns and one monthly sampling campaign during June 2010-May 2011 were carried out to investigate the CH4 flux across the water-gas interface in Xiangxi Bay of the Three Gorges Reservoir, China. The average CH4 flux was much less than that reported from reservoirs in tropic and temperate regions. The photosynthesis of phytoplankton dominated the diel gas fluxes during alga bloom in spring and summer. The maximum monthly flux occurred in June 2010 and corresponded to the lowest water level. Water temperature, sediment temperature, and TOC did not have significant correlation with the monthly CH4 fluxes. Continuously decreasing hydrostatic pressure and the low water level resulted in more CH4 emission at the sediment-water during the discharging period, and thus increases the CH4 effluxes because the diffusion time through a thin water column is shorter and less CH4 may be oxidized compared with that in a long water column.
Project description:Pseudo-nitzschia blooms often occur in coastal and open ocean environments, sometimes leading to the production of the neurotoxin domoic acid that can cause severe negative impacts to higher trophic levels. Increasing evidence suggests a close relationship between phytoplankton bloom and bacterial assemblages, however, the microbial composition and succession during a bloom process is unknown. Here, we investigate the bacterial assemblages before, during and after toxic and non-toxic Pseudo-nitzschia blooms to determine the patterns of bacterial succession in a natural bloom setting. Opportunistic sampling of bacterial community profiles were determined weekly at Santa Cruz Municipal Wharf by 454 pyrosequencing and analyzed together with domoic acid levels, phytoplankton community and biomass, nutrients and temperature. We asked if the bacterial communities are similar between bloom and non-bloom events and if domoic acid or the presence of toxic algal species acts as a driving force that can significantly structure phytoplankton-associated bacterial communities. We found that bacterial diversity generally increases when Pseudo-nitzschia numbers decline. Furthermore, bacterial diversity is higher when the low-DA producing P. fraudulenta dominates the algal bloom while bacterial diversity is lower when high-DA producing P. australis dominates the algal bloom, suggesting that the presence of algal toxin can structure bacterial community. We also found bloom-related succession patterns among associated bacterial groups; Gamma-proteobacteria, were dominant during low toxic P. fraudulenta blooms comprising mostly of Vibrio spp., which increased in relative abundance (6-65%) as the bloom progresses. On the other hand, Firmicutes bacteria comprising mostly of Planococcus spp. (12-86%) dominate during high toxic P. australis blooms, with the bacterial assemblage showing the same bloom-related successional patterns in three independent bloom events. Other environmental variables such as nitrate and phosphate and temperature appear to influence some low abundant bacterial groups as well. Our results suggest that phytoplankton-associated bacterial communities are strongly affected not just by phytoplankton bloom in general, but also by the type of algal species that dominates in the natural bloom.
Project description:Phytoplankton blooms are an important, widespread phenomenon in open oceans, coastal waters and freshwaters, supporting food webs and essential ecosystem services. Blooms are even more important in exploited coastal waters for maintaining high resource production. However, the environmental factors driving blooms in shallow productive coastal waters are still unclear, making it difficult to assess how environmental fluctuations influence bloom phenology and productivity. To gain insights into bloom phenology, Chl a fluorescence and meteorological and hydrological parameters were monitored at high-frequency (15 min) and nutrient concentrations and phytoplankton abundance and diversity, were monitored weekly in a typical Mediterranean shallow coastal system (Thau Lagoon). This study was carried out from winter to late spring in two successive years with different climatic conditions: 2014/2015 was typical, but the winter of 2015/2016 was the warmest on record. Rising water temperature was the main driver of phytoplankton blooms. However, blooms were sometimes correlated with winds and sometimes correlated with salinity, suggesting nutrients were supplied by water transport via winds, saltier seawater intake, rain and water flow events. This finding indicates the joint role of these factors in determining the success of phytoplankton blooms. Furthermore, interannual variability showed that winter water temperature was higher in 2016 than in 2015, resulting in lower phytoplankton biomass accumulation in the following spring. Moreover, the phytoplankton abundances and diversity also changed: cyanobacteria (< 1 ?m), picoeukaryotes (< 1 ?m) and nanoeukaryotes (3-6 ?m) increased to the detriment of larger phytoplankton such as diatoms. Water temperature is a key factor affecting phytoplankton bloom dynamics in shallow productive coastal waters and could become crucial with future global warming by modifying bloom phenology and changing phytoplankton community structure, in turn affecting the entire food web and ecosystem services.
Project description:Two annual Baltic Sea phytoplankton blooms occur in spring and summer. The bloom intensity is determined by nutrient concentrations in the water, while the period depends on weather conditions. During the course of the bloom, dead cells sink to the sediment where their degradation consumes oxygen to create hypoxic zones (<?2 mg/L dissolved oxygen). These zones prevent the establishment of benthic communities and may result in fish mortality. The aim of the study was to determine how the spring and autumn sediment chemistry and microbial community composition changed due to degradation of diatom or cyanobacterial biomass, respectively. Results from incubation of sediment cores showed some typical anaerobic microbial processes after biomass addition such as a decrease in NO2-?+?NO3- in the sediment surface (0-1 cm) and iron in the underlying layer (1-2 cm). In addition, an increase in NO2-?+?NO3- was observed in the overlying benthic water in all amended and control incubations. The combination of NO2-?+?NO3- diffusion plus nitrification could not account for this increase. Based on 16S rRNA gene sequences, the addition of cyanobacterial biomass during autumn caused a large increase in ferrous iron-oxidizing archaea while diatom biomass amendment during spring caused minor changes in the microbial community. Considering that OTUs sharing lineages with acidophilic microorganisms had a high relative abundance during autumn, it was suggested that specific niches developed in sediment microenvironments. These findings highlight the importance of nitrogen cycling and early microbial community changes in the sediment due to sinking phytoplankton before potential hypoxia occurs.
Project description:Early spring phytoplankton blooms can occur at very low water temperatures but they are often decoupled from bacterial growth, which is assumed to be often temperature controlled. In a previous mesocosm study with Baltic Sea plankton communities, an early diatom bloom was associated with a high relative abundance of Glaciecola sequences (Gammaproteobacteria), at both low (2°C) and elevated (8°C) temperatures, suggesting an important role for this genus in phytoplankton-bacteria coupling. In this study, the temperature-dependent dynamics of free-living Glaciecola spp. during the bloom were analyzed by catalyzed reporter deposition fluorescence in situ hybridization using a newly developed probe. The analysis revealed the appearance of Glaciecola spp. in this and in previous spring mesocosm experiments as the dominating bacterial clade during diatom blooms, with a close coupling between the population dynamics of Glaciecola and phytoplankton development. Although elevated temperature resulted in a higher abundance and a higher net growth rate of Glaciecola spp. (Q10 ? 2.2), their growth was, in contrast to that of the bulk bacterial assemblages, not suppressed at 2°C and showed a similar pattern at 8°C. Independent of temperature, the highest abundance of Glaciecola spp. (24.0 ± 10.0% of total cell number) occurred during the peak of the phytoplankton bloom. Together with the slightly larger cell size of Glaciecola, this resulted in a ?30% contribution of Glaciecola to total bacterial biomass. Overall, the results of this and previous studies suggest that Glaciecola has an ecological niche during early diatom blooms at low temperatures, when it becomes a dominant consumer of phytoplankton-derived dissolved organic matter.
Project description:Research so far has provided little evidence that benthic biogeochemical cycling is affected by ocean acidification under realistic climate change scenarios. We measured nutrient exchange and sediment community oxygen consumption (SCOC) rates to estimate nitrification in natural coastal permeable and fine sandy sediments under pre-phytoplankton bloom and bloom conditions. Ocean acidification, as mimicked in the laboratory by a realistic pH decrease of 0.3, significantly reduced SCOC on average by 60% and benthic nitrification rates on average by 94% in both sediment types in February (pre-bloom period), but not in April (bloom period). No changes in macrofauna functional community (density, structural and functional diversity) were observed between ambient and acidified conditions, suggesting that changes in benthic biogeochemical cycling were predominantly mediated by changes in the activity of the microbial community during the short-term incubations (14 days), rather than by changes in engineering effects of bioturbating and bio-irrigating macrofauna. As benthic nitrification makes up the gross of ocean nitrification, a slowdown of this nitrogen cycling pathway in both permeable and fine sediments in winter, could therefore have global impacts on coupled nitrification-denitrification and hence eventually on pelagic nutrient availability.