Annual Dynamics of Phytoplankton in the Black Sea in Relation to Wind Exposure

Studies of the annual dynamics of phytoplankton in the NE Black Sea at two stations on the shelf and the continental slope were conducted in 2016, 2017, and 2019. The species composition of phytoplankton has not undergone significant changes compared to previous decades. The coccolithophore Emiliania huxleyi, small flagellates, and diatoms determined the abundance of phytoplankton; and diatoms, coccolithophores, and dinoflagellates determined the total biomass. The annual dynamics of the satellite-derived chlorophyll-a showed peaks in spring and autumn, and sometimes in summer. During the stratified water column period, strong winds in most cases led to a detectible increase in chlorophyll-a. The annual dynamics of phytoplankton followed the pattern: small diatoms (spring) → coccolithophores (late spring, early summer) → large diatoms (summer, autumn). Such a pattern was typical for the previous decades. Coccolithophores dominated in weak SE winds, diatoms in NE winds. The combined effect of sustained offshore wind and strong current can cause diatom blooms during stratified water, even if the wind velocity is moderate.

Impact of Shifting Subpolar Front on Phytoplankton Dynamics in the Western Margin of East/Japan Sea

A subpolar front (SPF) generated between the East Korea Warm Current (EKWC) and the North Korea Cold Current (NKCC) in the western margin of the East/Japan Sea has shifted northward in recent decades. This study investigated the biomass and composition of the phytoplankton assemblage in relation to hydrological and biogeochemical features in the shallow shelf and slope off the Korean coast from January to June in 2016 and 2017, to determine the mechanistic effects of SPF on spring–summer phytoplankton bloom dynamics. Monthly average depth-integrated chlorophyll a (Chl a) levels and the contribution of phytoplankton classes revealed bimodal diatom blooms in early spring and summer in the frontal zone. Canonical correspondence analysis showed that the distribution of high Chl a was associated with cold, low-salinity NKCC water in March 2016. No Chl a peak was observed in March 2017 when the warm saline EKWC water mass invaded. These results suggest that the NKCC intrusion acts as a forcing mechanism leading to enhanced phytoplankton biomass in the frontal zone. In contrast, positive correlations of Chl a concentration with water density and nutrient concentrations suggest that summer blooms were fed by the subsurface chlorophyll maximum (SCM) driven by shoaling of the pycnocline and nitracline. Varying water-column stratification determined the thickness of the SCM layer, driving year-to-year variability in the magnitude of diatom blooms. These findings further suggest that seasonal/interannual variability in the timing of algal blooms affects regional trophodynamics and hence could be an important factor in explaining ecosystem changes in this region.

Large diatom bloom off the Antarctic Peninsula during cool conditions associated with the 2015/2016 El Niño

Diatoms play crucial functions in trophic structure and biogeochemical cycles. Due to poleward warming, there has been a substantial decrease in diatom biomass, especially in Antarctic regions that experience strong physical changes. Here we analyze the phytoplankton contents of water samples collected in the spring/summer of 2015/2016 off the North Antarctic Peninsula during the extreme El Niño event and compare them with corresponding satellite chlorophyll-a data. The results suggest a close link between large diatom blooms, upper ocean physical structures and sea ice cover, as a consequence of the El Niño effects. We observed massive concentrations (up to 40 mg m–3 of in situ chlorophyll-a) of diatoms coupled with substantially colder atmospheric and oceanic temperatures and high mean salinity values associated with a lower input of meltwater. We hypothesize that increased meltwater concentration due to continued atmospheric and oceanic warming trends will lead to diatom blooms becoming more episodic and spatially/temporally restricted.

Chlorophyll fluorescence as a light signal enhances iron uptake by the marine diatom Phaeodactylum tricornutum under high-cell density conditions

Background Diatoms usually dominate phytoplankton blooms in open oceans, exhibiting extremely high population densities. Although the iron uptake rate of diatoms largely determines the magnitude and longevity of diatom blooms, the underlying mechanisms regulating iron uptake remain unclear. Results The transcription of two iron uptake proteins, ISIP2a and ISIP1, in the marine diatom Phaeodactylum tricornutum was enhanced with increasing cell density, whereas the cellular iron content showed the opposite trend. When compared with the wild-type strain, knockdown of ISIP2a resulted in 43% decrease in cellular iron content, implying the involvement of ISIP2a in iron uptake under high-cell density conditions. Incubation of the diatom cells with sonicated cell lysate conditioned by different cell densities did not affect ISIP2a and ISIP1 expression, ruling out regulation via chemical cues. In contrast, ISIP2a and ISIP1 transcription were strongly induced by red light. Besides, chlorophyll fluorescence excited from the blue light was also positively correlated with population density. Subsequently, a “sandwich” illumination incubator was designed to filter out stray light and ensure that the inner layer cells only receive the emitted chlorophyll fluorescence from outer layers, and the results showed that the increase in outer cell density significantly elevated ISIP2a and ISIP1 transcription in inner layer cells. In situ evidence from Tara oceans also showed positively correlated between diatom ISIP transcripts and chlorophyll content. Conclusions This study shows that chlorophyll fluorescence derived from neighboring cells is able to upregulate ISIP2a and ISIP1 expression to facilitate iron assimilation under high-cell density. These results provide novel insights into biotic signal sensing in phytoplankton, which can help to elucidate the underlying mechanisms of marine diatom blooms.

Is a High Abundance of Spring Diatoms in the Photic Zone of Lake Baikal in July 2019 Due to an Upwelling Event?

A high abundance of planktonic microalgae is typically thought to be related to their ‘bloom’, that is, to active population growth. Diatom blooms in the photic zone of Lake Baikal generally occur during hydrological spring (April–June); when the summer arrives and the surface water temperature increases, diatoms are replaced by other microalgae. In July 2019, we found a concentration of the diatom Fragilaria radians at a station in South Baikal that was extremely high for that season. This species generally blooms in spring, but in spring (May) of 2019, this alga was nearly absent from the phytoplankton population. Microscopic analysis of the sample taken in July 2019 revealed that the cells were in a dormant stage. The species composition of microalgae in phytoplankton samples from May 2018 and July 2019 was similar. According to the temperature profile analysis, a summer upwelling event from a depth of ca. 100 m occurred in 2019. We hypothesised that this event caused the resuspension of microalgae, including Fragilaria radians, which were deposited on the slopes of the lake in 2018. Hence, the high abundance is not always a ‘bloom’ or an active growth.

Verrucomicrobiota are specialist consumers of sulfated methyl pentoses during diatom blooms

Marine algae annually sequester petagrams of carbon dioxide into polysaccharides, which are a central metabolic fuel for marine carbon cycling. Diatom microalgae produce sulfated polysaccharides containing methyl pentoses that are challenging to degrade for bacteria compared to other monomers, implicating these sugars as a potential carbon sink. Free-living bacteria occurring in phytoplankton blooms that specialise on consuming microalgal sugars, containing fucose and rhamnose remain unknown. Here, genomic and proteomic data indicate that small, coccoid, free-living Verrucomicrobiota specialise in fucose and rhamnose consumption during spring algal blooms in the North Sea. Verrucomicrobiota cell abundance was coupled with the algae bloom onset and accounted for up to 8% of the bacterioplankton. Glycoside hydrolases, sulfatases, and bacterial microcompartments, critical proteins for the consumption of fucosylated and sulfated polysaccharides, were actively expressed during consecutive spring bloom events. These specialised pathways were assigned to novel and discrete candidate species of the Akkermansiaceae and Puniceicoccaceae families, which we here describe as Candidatus Mariakkermansia forsetii and Candidatus Fucivorax forsetii. Moreover, our results suggest specialised metabolic pathways could determine the fate of complex polysaccharides consumed during algae blooms. Thus the sequestration of phytoplankton organic matter via methyl pentose sugars likely depend on the activity of specialised Verrucomicrobiota populations.

Role of nearshore benthic algae in the Lake Michigan silica cycle

Si cycling is linked with processes from global carbon sequestration to community composition and is especially important in aquatic ecosystems. Lake Michigan has seen dramatic fluctuations in dissolved silica (dSi) over several decades, which have been examined in the context of planktonic processes (diatom blooms), but the role of benthic organisms (macroalgae and their epiphytes) in Si cycling have not been explored. To assess significance of nearshore benthic algae in Si dynamics, we assembled dSi data from an offshore site sampled since the late 1980’s, and sampled off three Milwaukee beaches during 2005–19. Using colorimetric assays and alkaline digestion, we measured dSi, biogenic silica in particulate suspended material (pSi) and biogenic silica in benthic macroalgae (Cladophora) and epiphytic diatoms (bSi). Offshore, dSi increased about 1 μM per year from 25 μM in the late 1980’s to nearly 40 μM in 2019. Nearshore dSi fluctuated dramatically annually, from near zero to concentrations similar to offshore. Both Cladophora and its epiphytes contained significant bSi, reaching up to 30% of dry mass (300 mg Si g dry mass-1) of the assemblage in summer. Microscopic analyses including localization with a Si-specific-stain and X-ray microanalysis showed bSi in epiphytic diatom cells walls, but the nature and localization of Si in macroalgae remained unclear. A simple model was developed estimating Si demand of algae using the areal macroalgal biomass, growth rates inferred from P-content, and bSi content, and comparing Si demand with dSi available in the water column. This indicated that 7–70% of the dSi in water overlying nearshore benthic algal beds could be removed per day. Key elements of the Si cycle, including which organisms sequester bSi and how rapidly Si is recycled, remain unclear. This work has implications for coastal marine waters where large macroalgal biomass accumulates but bSi content is virtually unknown.

Tight Adherence (Tad) Pilus Genes Indicate Putative Niche Differentiation in Phytoplankton Bloom Associated Rhodobacterales

The multiple interactions of phytoplankton and bacterioplankton are central for our understanding of aquatic environments. A prominent example of those is the consistent association of diatoms with Alphaproteobacteria of the order Rhodobacterales. These photoheterotrophic bacteria have traditionally been described as generalists that scavenge dissolved organic matter. Many observations suggest that members of this clade are specialized in colonizing the microenvironment of diatom cells, known as the phycosphere. However, the molecular mechanisms that differentiate Rhodobacterales generalists and phycosphere colonizers are poorly understood. We investigated Rhodobacterales in the North Sea during the 2010–2012 spring blooms using a time series of 38 deeply sequenced metagenomes and 10 metaproteomes collected throughout these events. Rhodobacterales metagenome assembled genomes (MAGs) were recurrently abundant. They exhibited the highest gene enrichment and protein expression of small-molecule transporters, such as monosaccharides, thiamine and polyamine transporters, and anaplerotic pathways, such as ethylmalonyl and propanoyl-CoA metabolic pathways, all suggestive of a generalist lifestyle. Metaproteomes indicated that the species represented by these MAGs were the dominant suppliers of vitamin B12 during the blooms, concomitant with a significant enrichment of genes related to vitamin B12 biosynthesis suggestive of association with diatom phycospheres. A closer examination of putative generalists and colonizers showed that putative generalists had persistently higher relative abundance throughout the blooms and thus produced more than 80% of Rhodobacterales transport proteins, suggesting rapid growth. In contrast, putative phycosphere colonizers exhibited large fluctuation in relative abundance across the different blooms and correlated strongly with particular diatom species that were dominant during the blooms each year. The defining feature of putative phycosphere colonizers is the presence of the tight adherence (tad) gene cluster, which is responsible for the assembly of adhesive pili that presumably enable attachment to diatom hosts. In addition, putative phycosphere colonizers possessed higher prevalence of secondary metabolite biosynthetic gene clusters, particularly homoserine lactones, which can regulate bacterial attachment through quorum sensing. Altogether, these findings suggest that while many members of Rhodobacterales are competitive during diatom blooms, only a subset form close associations with diatoms by colonizing their phycospheres.

Harmful algal blooms and environmentally friendly control strategies in Japan

The presence and status of harmful algal blooms (HABs) in Japan are reviewed, revealing a decrease in red tides; however, toxic blooms are found to be increasing in western Japan. Environmentally friendly control strategies against HABs are also compared with integrated agricultural pest management. Very high densities (105–108 CFU/g) of algicidal and growth-inhibiting bacteria were found in biofilm on seagrass and seaweed surfaces and in surrounding coastal seawater. The situation in freshwater ecosystems is similar to coastal seas for toxic cyanobacterium, Microcystis aeruginosa, and aquatic plants. These findings offer new insights into the ecology of influential bacteria and harmful algae, suggesting that protection and restoration of native seagrasses and seaweeds in coastal marine environments should be implemented to suppress HABs. Diatom blooms were successfully induced with bottom sediment perturbation to prevent the occurrence of harmful flagellates such as Chattonella spp. and Alexandrium catenella in the Seto Inland Sea; however, this method requires robust and reproducible verification. “Sato-Umi” is a helpful concept for HAB control in the sea and freshwater ecosystems when adequately managed by people (e.g., appropriate bottom perturbation; protection and restoration of seaweeds, seagrasses, and aquatic plants; application of polycultures of fish, seaweeds, etc.).

Representative Diatom and Coccolithophore Species Exhibit Divergent Responses throughout Simulated Upwelling Cycles

ABSTRACT Wind-driven upwelling followed by relaxation results in cycles of cold nutrient-rich water fueling intense phytoplankton blooms followed by nutrient depletion, bloom decline, and sinking of cells. Surviving cells at depth can then be vertically transported back to the surface with upwelled waters to seed another bloom. As a result of these cycles, phytoplankton communities in upwelling regions are transported through a wide range of light and nutrient conditions. Diatoms appear to be well suited for these cycles, but their responses to them remain understudied. To investigate the bases for diatoms’ ecological success in upwelling environments, we employed laboratory simulations of a complete upwelling cycle with a common diatom, Chaetoceros decipiens, and coccolithophore, Emiliania huxleyi. We show that while both organisms exhibited physiological and transcriptomic plasticity, the diatom displayed a distinct response enabling it to rapidly shift-up growth rates and nitrate assimilation when returned to light and available nutrients following dark nutrient-deplete conditions. As observed in natural diatom communities, C. decipiens highly expresses before upwelling, or frontloads, key transcriptional and nitrate assimilation genes, coordinating its rapid response to upwelling conditions. Low-iron simulations showed that C. decipiens is capable of maintaining this response when iron is limiting to growth, whereas E. huxleyi is not. Differential expression between iron treatments further revealed specific genes used by each organism under low iron availability. Overall, these results highlight the responses of two dominant phytoplankton groups to upwelling cycles, providing insight into the mechanisms fueling diatom blooms during upwelling events. IMPORTANCE Coastal upwelling regions are among the most biologically productive ecosystems. During upwelling events, nutrient-rich water is delivered from depth resulting in intense phytoplankton blooms typically dominated by diatoms. Along with nutrients, phytoplankton may also be transported from depth to seed these blooms then return to depth as upwelling subsides creating a cycle with varied conditions. To investigate diatoms’ success in upwelling regions, we compare the responses of a common diatom and coccolithophore throughout simulated upwelling cycles under iron-replete and iron-limiting conditions. The diatom exhibited a distinct rapid response to upwelling irrespective of iron status, whereas the coccolithophore’s response was either delayed or suppressed depending on iron availability. Concurrently, the diatom highly expresses, or frontloads, nitrate assimilation genes prior to upwelling, potentially enabling this rapid response. These results provide insight into the molecular mechanisms underlying diatom blooms and ecological success in upwelling regions.