Seasonal Succession of Free-Living Bacterial Communities in Coastal Waters of the Western Antarctic Peninsula.
ABSTRACT: The marine ecosystem along the Western Antarctic Peninsula undergoes a dramatic seasonal transition every spring, from almost total darkness to almost continuous sunlight, resulting in a cascade of environmental changes, including phytoplankton blooms that support a highly productive food web. Despite having important implications for the movement of energy and materials through this ecosystem, little is known about how these changes impact bacterial succession in this region. Using 16S rRNA gene amplicon sequencing, we measured changes in free-living bacterial community composition and richness during a 9-month period that spanned winter to the end of summer. Chlorophyll a concentrations were relatively low until summer when a major phytoplankton bloom occurred, followed 3 weeks later by a high peak in bacterial production. Richness in bacterial communities varied between ~1,200 and 1,800 observed operational taxonomic units (OTUs) before the major phytoplankton bloom (out of ~43,000 sequences per sample). During peak bacterial production, OTU richness decreased to ~700 OTUs. The significant decrease in OTU richness only lasted a few weeks, after which time OTU richness increased again as bacterial production declined toward pre-bloom levels. OTU richness was negatively correlated with bacterial production and chlorophyll a concentrations. Unlike the temporal pattern in OTU richness, community composition changed from winter to spring, prior to onset of the summer phytoplankton bloom. Community composition continued to change during the phytoplankton bloom, with increased relative abundance of several taxa associated with phytoplankton blooms, particularly Polaribacter. Bacterial community composition began to revert toward pre-bloom conditions as bacterial production declined. Overall, our findings clearly demonstrate the temporal relationship between phytoplankton blooms and seasonal succession in bacterial growth and community composition. Our study highlights the importance of high-resolution time series sampling, especially during the relatively under-sampled Antarctic winter and spring, which enabled us to discover seasonal changes in bacterial community composition that preceded the summertime phytoplankton bloom.
Project description:In temperate systems, phytoplankton spring blooms deplete inorganic nutrients and are major sources of organic matter for the microbial loop. In response to phytoplankton exudates and environmental factors, heterotrophic microbial communities are highly dynamic and change their abundance and composition both on spatial and temporal scales. Yet, most of our understanding about these processes comes from laboratory model organism studies, mesocosm experiments or single temporal transects. Spatial-temporal studies examining interactions of phytoplankton blooms and bacterioplankton community composition and function, though being highly informative, are scarce. In this study, pelagic microbial community dynamics (bacteria and phytoplankton) and environmental variables were monitored during a spring bloom across the Baltic Proper (two cruises between North Germany to Gulf of Finland). To test to what extent bacterioplankton community composition relates to the spring bloom, we used next generation amplicon sequencing of the 16S rRNA gene, phytoplankton diversity analysis based on microscopy counts and population genotyping of the dominating diatom Skeletonema marinoi. Several phytoplankton bloom related and environmental variables were identified to influence bacterial community composition. Members of Bacteroidetes and Alphaproteobacteria dominated the bacterial community composition but the bacterial groups showed no apparent correlation with direct bloom related variables. The less abundant bacterial phyla Actinobacteria, Planctomycetes, and Verrucomicrobia, on the other hand, were strongly associated with phytoplankton biomass, diatom:dinoflagellate ratio, and colored dissolved organic matter (cDOM). Many bacterial operational taxonomic units (OTUs) showed high niche specificities. For example, particular Bacteroidetes OTUs were associated with two distinct genetic clusters of S. marinoi. Our study revealed the complexity of interactions of bacterial taxa with inter- and intraspecific genetic variation in phytoplankton. Overall, our findings imply that biotic and abiotic factors during spring bloom influence bacterial community dynamics in a hierarchical manner.
Project description:Carbohydrates represent an important fraction of labile and semi-labile marine organic matter that is mainly comprised of exopolymeric substances derived from phytoplankton exudation and decay. This study investigates the composition of total combined carbohydrates (tCCHO; >1 kDa) and the community development of free-living (0.2-3 ?m) and particle-associated (PA) (3-10 ?m) bacterioplankton during a spring phytoplankton bloom in the southern North Sea. Furthermore, rates were determined for the extracellular enzymatic hydrolysis that catalyzes the initial step in bacterial organic matter remineralization. Concentrations of tCCHO greatly increased during bloom development, while the composition showed only minor changes over time. The combined concentration of glucose, galactose, fucose, rhamnose, galactosamine, glucosamine, and glucuronic acid in tCCHO was a significant factor shaping the community composition of the PA bacteria. The richness of PA bacteria greatly increased in the post-bloom phase. At the same time, the increase in extracellular ?-glucosidase activity was sufficient to explain the observed decrease in tCCHO, indicating the efficient utilization of carbohydrates by the bacterioplankton community during the post-bloom phase. Our results suggest that carbohydrate concentration and composition are important factors in the multifactorial environmental control of bacterioplankton succession and the enzymatic hydrolysis of organic matter during phytoplankton blooms.
Project description:The North Atlantic phytoplankton spring bloom is the pinnacle in an annual cycle that is driven by physical, chemical, and biological seasonality. Despite its important contributions to the global carbon cycle, transitions in plankton community composition between the winter and spring have been scarcely examined in the North Atlantic. Phytoplankton composition in early winter was compared with latitudinal transects that captured the subsequent spring bloom climax. Amplicon sequence variants (ASVs), imaging flow cytometry, and flow-cytometry provided a synoptic view of phytoplankton diversity. Phytoplankton communities were not uniform across the sites studied, but rather mapped with apparent fidelity onto subpolar- and subtropical-influenced water masses of the North Atlantic. At most stations, cells?<?20-µm diameter were the main contributors to phytoplankton biomass. Winter phytoplankton communities were dominated by cyanobacteria and pico-phytoeukaryotes. These transitioned to more diverse and dynamic spring communities in which pico- and nano-phytoeukaryotes, including many prasinophyte algae, dominated. Diatoms, which are often assumed to be the dominant phytoplankton in blooms, were contributors but not the major component of biomass. We show that diverse, small phytoplankton taxa are unexpectedly common in the western North Atlantic and that regional influences play a large role in modulating community transitions during the seasonal progression of blooms.
Project description:Temperate coastal marine environments are replete with complex biotic and abiotic interactions that are amplified during spring and summer phytoplankton blooms. During these events, heterotrophic bacterioplankton respond to successional releases of dissolved organic matter as algal cells are lysed. Annual seasonal shifts in the community composition of free-living bacterioplankton follow broadly predictable patterns, but whether similar communities respond each year to bloom disturbance events remains unknown owing to a lack of data sets, employing high-frequency sampling over multiple years. We capture the fine-scale microdiversity of these events with weekly sampling using a high-resolution method to discriminate 16S ribosomal RNA gene amplicons that are >99% identical. Furthermore, we used 2 complete years of data to facilitate identification of recurrent sub-networks of co-varying microbes. We demonstrate that despite inter-annual variation in phytoplankton blooms and despite the dynamism of a coastal-oceanic transition zone, patterns of microdiversity are recurrent during both bloom and non-bloom conditions. Sub-networks of co-occurring microbes identified reveal that correlation structures between community members appear quite stable in a seasonally driven response to oligotrophic and eutrophic conditions.
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:Many freshwater phytoplankton species have the potential to form transient nuisance blooms that affect water quality and other aquatic biota. Heterotrophic bacteria can influence such blooms via nutrient regeneration but also via antagonism and other biotic interactions. We studied the composition of bacterial communities associated with three bloom-forming freshwater phytoplankton species, the diatom Aulacoseira granulata and the cyanobacteria Microcystis aeruginosa and Cylindrospermopsis raciborskii. Experimental cultures incubated with and without lake bacteria were sampled in three different growth phases and bacterial community composition was assessed by 454-Pyrosequencing of 16S rRNA gene amplicons. Betaproteobacteria were dominant in all cultures inoculated with lake bacteria, but decreased during the experiment. In contrast, Alphaproteobacteria, which made up the second most abundant class of bacteria, increased overall during the course of the experiment. Other bacterial classes responded in contrasting ways to the experimental incubations causing significantly different bacterial communities to develop in response to host phytoplankton species, growth phase and between attached and free-living fractions. Differences in bacterial community composition between cyanobacteria and diatom cultures were greater than between the two cyanobacteria. Despite the significance, major differences between phytoplankton cultures were in the proportion of the OTUs rather than in the absence or presence of specific taxa. Different phytoplankton species favoring different bacterial communities may have important consequences for the fate of organic matter in systems where these bloom forming species occur. The dynamics and development of transient blooms may also be affected as bacterial communities seem to influence phytoplankton species growth in contrasting ways.
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: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:Bacterial communities are an important part of biological diversity and biogeochemical cycling in aquatic ecosystems. In this study, the relationship amongst the phytoplankton species composition and abiotic environmental factors on seasonal changes in the community composition of free-living and attached bacteria in Lake Erhai were studied. Using Illumina high-throughput sequencing, we found that the impact of environmental factors on both the free-living and attached bacterial community composition was greater than that of the phytoplankton community, amongst which total phosphorus, Secchi disk, water temperature, dissolved oxygen and conductivity strongly influenced bacterial community composition. Microcystis blooms associated with subdominant Psephonema occurred during the summer and autumn, and Fragilaria, Melosira and Mougeotia were found at high densities in the other seasons. Only small numbers of algal species-specific bacteria, including Xanthomonadaceae (Proteobacteria) and Alcaligenaceae (Betaproteobacteria), were tightly coupled to Microcystis and Psephonema during Microcystis blooms. Redundancy analysis showed that although the composition of the bacterial communities was controlled by species composition mediated by changes in phytoplankton communities and abiotic environmental factors, the impact of the abiotic environment on both free-living and attached bacterial community compositions were greater than the impact of the phytoplankton community. These results suggest that the species composition of both free-living and attached bacterial communities are affected by abiotic environmental factors, even when under strong control by biotic factors, particularly dominant genera of Microcystis and Psephonema during algal blooms.
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.