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Thaumarchaeota and Thermoplasmatota are the most abundant planktonic archaea in the sea. Thaumarchaeota contain tetraether lipids as their major membrane lipids, but the lipid composition of uncultured planktonic Thermoplasmatota representatives remains unknown. To address this knowledge gap, we quantified archaeal cells and ether lipids in open ocean depth profiles (0–200 m) of the North Pacific Subtropical Gyre. Planktonic archaeal community structure and ether lipid composition in the water column partitioned into two separate clusters: one above the deep chlorophyll maximum, the other within and below it. In surface waters, Thermoplasmatota densities ranged from 2.11 × 106 to 6.02 × 106 cells/L, while Thaumarchaeota were undetectable. As previously reported for Thaumarchaeota, potential homologs of archaeal tetraether ring synthases were present in planktonic Thermoplasmatota metagenomes. Despite the absence of Thaumarchaeota in surface waters, measurable amounts of intact polar ether lipids were found there. Based on cell abundance estimates, these surface water archaeal ether lipids contributed only 1.21 × 10–9 ng lipid/Thermoplasmatota cell, about three orders of magnitude less than that reported for Thaumarchaeota cells. While these data indicate that even if some tetraether and diether lipids may be derived from Thermoplasmatota, they would only comprise a small fraction of Thermoplasmatota total biomass. Therefore, while both MGI Thaumarchaeota and MGII/III Thermoplasmatota are potential biological sources of archaeal GDGTs, the Thaumarchaeota appear to be the major contributors of archaeal tetraether lipids in planktonic marine habitats. These results extend and confirm previous reports of planktonic archaeal lipid sources, and further emphasize the need for Thermoplasmatota cultivation, to better characterize the membrane lipid constituents of marine planktonic Thermoplasmatota, and more precisely define the sources and patterns of archaeal tetraether lipid distributions in marine plankton.

Solubilized particulate organic matter (POM) rather than dissolved organic matter (DOM) has been speculated to be the major carbon and energy sources for heterotrophic prokaryotes in the ocean. However, the direct evidence is still lack. Here we characterized microbial transport proteins of POM collected from both euphotic (75 m, deep chlorophyll maximum DCM, and 100 m) and upper-twilight (200 m and 500 m) zones in three contrasting environments in the northwest Pacific Ocean using a metaproteomic approach. The proportion of transport proteins was relatively high at the bottom of the euphotic zone (200 m), indicating that this layer was the most active area of microbe-driven POM remineralization in the water column. In the upper-twilight zone, the predicted substrates of the identified transporters indicated that amino acids, carbohydrates, taurine, inorganic nutrients, urea, biopolymers, and cobalamin were essential substrates for the microbial community. SAR11, Rhodobacterales, Alteromonadales, and Enterobacteriales were the key contributors with the highest expression of transporters. Interestingly, both the taxonomy and function of the microbial communities varied among water layers and sites with different environments; however, the distribution of transporter types and their relevant organic substrates were similar among samples, suggesting that microbial communities took up similar compounds and were functionally redundant in organic matter utilization throughout the water column. The similar vertical distribution of transport proteins from the euphotic zone to the upper twilight zone among the contrasting environments indicated that solubilized POM rather than DOM was the preferable carbon and energy sources for the microbial communities.

Mesoscale eddies can have a strong impact on regional biogeochemistry and primary productivity. To investigate the effect of the upwelling of seawater by western Pacific eddies on the composition of the active planktonic marine archaeal community composition of the deep chlorophyll maximum (DCM) layer, mesoscale cold-core eddies were simulated in situ by mixing western Pacific DCM layer water with mesopelagic layer (400 m) water. Illumina sequencing of the 16S rRNA gene and 16S rRNA transcripts indicated that the specific heterotrophic Marine Group IIb (MGIIb) taxonomic group of the DCM layer was rapidly stimulated after receiving fresh substrate from 400 m water, which was dominated by uncultured autotrophic Marine Group I (MGI) archaea. Furthermore, niche differentiation of autotrophic ammonia-oxidizing archaea (MGI) was demonstrated by deep sequencing of 16S rRNA, amoA, and accA genes, respectively. Similar distribution patterns of active Marine Group III (MGIII) were observed in the DCM layer with or without vertical mixing, indicating that they are inclined to utilize the substrates already present in the DCM layer. These findings underscore the importance of mesoscale cyclonic eddies in stimulating microbial processes involved in the regional carbon cycle.

Surface microbial communities are exposed to seasonally changing environmental conditions, resulting in recurring patterns of community composition. However, knowledge on temporal dynamics of open ocean microbial communities remains scarce. Seasonal patterns and associations of taxa and oligotypes from surface and chlorophyll maximum layers in the western Mediterranean Sea were studied over a 2-year period. Summer stratification versus winter mixing governed not only the prokaryotic community composition and diversity but also the temporal dynamics and co-occurrence association networks of oligotypes. Flavobacteriales, Rhodobacterales, SAR11, SAR86, and Synechococcales oligotypes exhibited contrasting seasonal dynamics, and consequently, specific microbial assemblages and potential inter-oligotype connections characterized the different seasons. In addition, oligotypes composition and dynamics differed between surface and deep chlorophyll maximum (DCM) prokaryotic communities, indicating depth-related environmental gradients as a major factor affecting association networks between closely related taxa. Taken together, the seasonal and depth specialization of oligotypes suggest temporal dynamics of community composition and metabolism, influencing ecosystem function and global biogeochemical cycles. Moreover, our results indicate highly specific associations between microbes, pointing to keystone ecotypes and fine-tuning of the microbes realized niche., SI

Many studies indicate that variation of marine bacterial beta diversity in the horizontal dimension is mainly attributable to environmental and spatial effects. However, whether and how these two effects drive bacterial beta diversity in the vertical dimension remains unclear, especially when considering seasonal variation in the strength of water stratification. Here, we used 78 paired bacterioplankton community samples from surface and deep chlorophyll maximum (DCM) layers along a transect in the Kuroshio region east of Taiwan across multiple seasons. Variance partitioning was used to evaluate the mechanisms driving the vertical beta diversity between surface-DCM bacterioplankton communities during weak stratification periods (i.e., spring and fall) versus strong stratification periods (i.e., summer). During strong periods of stratification, vertical beta diversity was shaped by both environmental and spatial effects; notably, the strength of stratification played an important role in enhancing environmental dissimilarity and creating a barrier to dispersal. In contrast, during periods of weak stratification, environmental effects dominate, with a non-significant spatial effect due to mixing. Variation of vertical beta diversity for bacterioplankton communities in the Kuroshio region east of Taiwan was structured by different mechanisms across seasons, and was further dependent on stratification strength of the water column.

The phytoplankton community composition, structure, and biomass were investigated under stratified and oligotrophic conditions during summer for three consecutive years in the Mediterranean Sea. Our results reveal that the phytoplankton community structure was strongly influenced by vertical stratification. The thermocline separated two different phytoplankton communities in the two layers of the euphotic zone, characterized by different nutrient and light availability. Picoplankton dominated in terms of abundance and biomass at all the stations sampled and throughout the photic zone. However, the structure of the picoplanktonic community changed with depth, with Synechococcus and heterotrophic prokaryotes dominating in surface waters down to the base of the thermocline, and Prochlorococcus and picoeukaryotes contributing relatively more to the community in the deep chlorophyll maximum (DCM). Light and nutrient availability also influenced the communities at the DCM layer. Prochlorococcus prevailed in deeper DCM waters characterized by lower light intensities and higher picophytoplankton abundance was related to lower nutrient concentrations at the DCM. Picoeukaryotes were the major phytoplankton contributors to carbon biomass at surface (up to 80%) and at DCM (more than 40%). Besides, contrarily to the other phytoplankton groups, picoeukaryotes cell size progressively decreased with depth. Our research shows that stratification is a major factor determining the phytoplankton community structure; and underlines the role that picoeukaryotes might play in the carbon flux through the marine food web, with implications for the community metabolism and carbon fate in the ecosystem., SI

Saharan dust input and seasonal upwelling along North-West Africa provide a model system for studying microbial processes related to the export and recycling of nutrients. This study offers the first molecular characterization of prokaryotic particle-attached (PA; >3.0 μm) and free-living (FL; 0.2-3.0 μm) players in this important ecosystem during August 2016. Environmental drivers for alpha-diversity, bacterial community composition, and differences between FL and PA fractions were identified. The ultra-oligotrophic waters off Senegal were dominated by Cyanobacteria while higher relative abundances of Alphaproteobacteria, Bacteroidetes, Verrucomicrobia, and Planctomycetes (known particle-degraders) occurred in the upwelling area. Temperature, proxy for different water masses, was the best predictor for changes in FL communities. PA community variation was best explained by temperature and ammonium. Bray Curtis dissimilarities between FL and PA were generally very high and correlated with temperature and salinity in surface waters. Greatest similarities between FL and PA occurred at the deep chlorophyll maximum, where bacterial substrate availability was likely highest. This indicates that environmental drivers do not only influence changes among FL and PA communities but also differences between them. This could provide an explanation for contradicting results obtained by different studies regarding the dissimilarity/similarity between FL and PA communities and their biogeochemical functions. Fil: Bachmann, Jennifer. Universitat Bremen; Alemania. Leibniz Centre for Tropical Marine Research; Alemania Fil: Heimbach, Tabea. Leibniz Centre for Tropical Marine Research; Alemania. Universitat Bremen; Alemania. Max Plank Institute for Marine Microbiology; Alemania Fil: Hassenrück, Christiane. Leibniz Centre for Tropical Marine Research; Alemania Fil: Kopprio, Germán Adolfo. Leibniz Centre for Tropical Marine Research; Alemania. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Bahía Blanca. Instituto Argentino de Oceanografía. Universidad Nacional del Sur. Instituto Argentino de Oceanografía; Argentina Fil: Iversen, Morten Hvitfeldt. Universitat Bremen; Alemania. Alfred Wegener Institute for Polar and Marine Research; Alemania Fil: Grossart, Hans Peter. Leibniz-Institute of Freshwater Ecology and Inland Fisheries; Alemania. University of Potsdam; Alemania Fil: Gärdes, Astrid. Leibniz Centre for Tropical Marine Research; Alemania

The deep sea is one of the largest but least understood ecosystems on earth. Knowledge about the diversity and distribution patterns as well as drivers of microbial eukaryote (including ciliates) along the water column, particularly below the photic zone, is scarce. In this study, we investigated the diversity of pelagic ciliates, the main group of marine microeukaryotes, their vertical distribution from the surface to the abyssopelagic zone, as well as their horizontal distribution over a distance of 1,300 km in the Western Pacific Ocean, using high-throughput DNA and cDNA (complementary DNA) sequencing. No distance-decay relationship could be detected along the horizontal scale; instead, a distinct vertical distribution within the ciliate communities was revealed. The alpha diversity of the ciliate communities in the deep chlorophyll maximum (DCM) and the 200 m layer turned out to be significantly higher compared with the other water layers. The ciliate communities in the 200 m water layer appeared to be more similar to those in deeper layers from 1,000 m to about 5,000 m than to the surface and DCM ciliate communities. Dominant species in the bathypelagic and abyssopelagic zone, particularly some parasites, were also detected in the 200 m layer, but were almost absent in the surface layer. The 200 m layer, therefore, seems to be an important “species bank” for deep ocean layers. Statistical analyses further revealed significant effects of temperature and chlorophyll a on the partitioning of ciliate diversity, indicating that environmental factors are a stronger force in shaping marine pelagic ciliate communities than the geographic distance.

This study characterizes viral and bacterial dynamics along a latitudinal transect in the Atlantic Ocean from approximately 10 N–40 S. Overall viral abundance decreased with depth, on average there were 1.64 ± 0.71 × 107 virus like particles (VLPs) in surface waters, decreasing to an average of 6.50 ± 2.26 × 105 VLPs in Antarctic Bottom Water. This decrease was highly correlated to bacterial abundance. There are six major water masses in the Southern Tropical Atlantic Ocean, and inclusion of water mass, temperature and salinity variables explained a majority of the variation in total viral abundance. Recent discovery of phages infecting bacteria of the SAR11 clade of Alphaproteobacteria (i.e., pelagiphages) leads to intriguing questions about the roles they play in shaping epipelagic communities. Viral-size fraction DNA from epipelagic water was used to quantify the abundance of two pelagiphages, using pelagiphage-specific quantitative PCR primers and probes along the transect. We found that HTVC010P, a member of a podoviridae sub-family, was most abundant in surface waters. Copy numbers ranged from an average of 1.03 ± 2.38 × 105 copies ml−1 in surface waters, to 5.79 ± 2.86 × 103 in the deep chlorophyll maximum. HTVC008M, a T4-like myovirus, was present in the deep chlorophyll maximum (5.42 ± 2.8 × 103 copies ml−1 on average), although it was not as highly abundant as HTVC010P in surface waters (6.05 ± 3.01 × 103 copies ml−1 on average). Interestingly, HTVC008M was only present at a few of the most southern stations, suggesting latitudinal biogeography of SAR11 phages.

The light effect on photoheterotrophic processes in Prochlorococcus, and primary and bacterial productivity in the oligotrophic North Pacific Subtropical Gyre was investigated using 14C-bicarbonate and 3H-leucine. Light and dark incubation experiments were conducted in situ throughout the euphotic zone (0-175 m) on nine expeditions to Station ALOHA over a three-year period. Photosynthetrons were also used to elucidate rate responses in leucine and inorganic carbon assimilation as a function of light intensity. Taxonomic group and cell-specific rates were assessed using flow cytometric sorting. The light:dark assimilation rate ratios of leucine in the top 150 m were ~7:1 for Prochlorococcus, whereas the light:dark ratio for the non-pigmented bacteria was not significant different from 1:1. Prochlorococcus assimilated leucine in the dark at per cell rates similar to the non-pigmented bacteria, with a contribution to the total community bacterial production, integrated over the euphotic zone, of approximately 20% in the dark and 60% in the light. Depth-resolved primary productivity and leucine incorporation showed that the ratio of Prochlorococcus leucine:primary production peaked at 100 m then declined steeply below the deep chlorophyll maximum (DCM). The photosynthetron experiments revealed that, for Prochlorococcus at the DCM, the saturating irradiance (Ek) for leucine incorporation was reached at approximately half the light intensity required for light saturation of 14C-bicarbonate assimilation. Additionally, high and low red fluorescing Prochlorococcus populations (HRF and LRF), co-occurring at the DCM, had similar Ek values for their respective substrates, however, maximum assimilation rates, for both leucine and inorganic carbon, were two times greater for HRF cells. Our results show that Prochlorococcus contributes significantly to bacterial production estimates using 3H-leucine, whether or not the incubations are conducted in the dark or light, and this should be considered when making assessments of bacterial production in marine environments where Prochlorococcus is present. Furthermore, Prochlorococcus primary productivity showed rate to light-flux patterns that were different from its light enhanced leucine incorporation. This decoupling from autotrophic growth may indicate a separate light stimulated mechanism for leucine acquisition.

Iron limits carbon fixation in much of the modern ocean due to the very low solubility of ferric iron in oxygenated ocean waters. We examined iron limitation of growth rate under varying light intensities in the coastal cyanobacterium Synechococcus bacillaris, a descendent of the oxygenic phototrophs that evolved ca. 3 billion years ago when the ocean was reducing and iron was present at much higher concentrations as soluble Fe(II). Decreasing light intensity increased the cellular iron:carbon (Fe:C) ratio needed to support a given growth rate, indicating that iron and light may co-limit the growth of Synechococcus in the ocean, as shown previously for eukaryotic phytoplankton. The cellular Fe:C ratios needed to support a given growth rate were 5- to 8-fold higher than ratios for coastal eukaryotic algae growing under the same light conditions. The higher iron requirements for growth in the coastal cyanobacterium may be largely caused by the high demand for iron in photosynthesis, and to higher ratios of iron-rich photosystem I to iron-poor photosystem II in Synechococcus than in eukaryotic algae. This high iron requirement may also be vestigial and represent an adaptation to the much higher iron levels in the ancient reducing ocean. Due to the high cellular iron requirement for photosynthesis and growth, and for low light acclimation, Synechococcus may be excluded from many low-iron and low-light environments. Indeed, it decreases rapidly with depth within the ocean’s deep chlorophyll maximum (DCM) where iron and light levels are low, and lower-iron requiring picoeukaryotes typically dominate the biomass of phytoplankton community within the mid to lower DCM.

The exploration of bacterial diversity in the global ocean has revealed new taxa and previously unrecognized metabolic potential; however, our understanding of what regulates this diversity is limited. Using terminal restriction fragment length polymorphism (T-RFLP) data of bacterial small-subunit ribosomal RNA genes we show that, independent of depth and time, a large fraction of bacterioplankton co-occurrence patterns are non-random in the oligotrophic North Pacific subtropical gyre (NPSG). Pair-wise correlations of all identified operational taxonomic units (OTUs) revealed a high degree of significance, with 6.6% of the pair-wise co-occurrences being negatively correlated and 20.7% of them being positive. The most abundant OTUs, putatively identified as Prochlorococcus, SAR11 and SAR116 bacteria, were among the most correlated OTUs. As expected, bacterial community composition lacked statistically significant patterns of seasonality in the mostly stratified water column except in a few depth horizons of the sunlit surface waters, with higher frequency variations in community structure apparently related to populations associated with the deep chlorophyll maximum. Communities were structured vertically, with a succession from euphotic, mesopelagic, and bathylopelagic populations. Permutation based statistical analyses of T-RFLP data and their corresponding metadata revealed a broad range of putative environmental drivers controlling bacterioplankton community composition in the NPSG, including concentrations of inorganic nutrients and phytoplankton pigment. Together our results suggest that deterministic forces, such as environmental filtering and interactions among taxa, determine bacterioplankton community patterns, and consequently affect ecosystem functions in the NPSG.

Planktothrix rubescensis a harmful planktonic cyanobacterium, forming concentrated metalimnetic populations in deep oligo- and mesotrophic lakes, even after successful restoration. In Lake Zurich (Switzerland),P. rubescensemerged as a keystone species with annual mass developments since the 1970s. Its success was partly attributed to effects of lake warming, such as changes in thermal stratification and seasonal deep mixing. However, recent observations based on a biweekly monitoring campaign (2009–2020) revealed two massive breakdowns and striking seasonal oscillations of the population. Here, we disentangle positive from negative consequences of secular lake warming and annual variations in weather conditions onP. rubescensdynamics: (i) despite the high survival rates of overwintering populations (up to 25%) during three consecutive winters (2014–2016) of incomplete deep convective mixing, cyanobacterial regrowth during the following stratified season was moderate and not overshooting a distinct standing stock threshold. Moreover, we recorded a negative trend for annual population maxima and total population size, pointing to a potential nutrient limitation after a series of incomplete winter mixing. Thus, the predication of steadily increasing blooms ofP. rubescenscould not be confirmed for the last decade. (ii) The seasonal reestablishment ofP. rubescenswas strongly coupled with a timely formation of a stable metalimnion structure, where the first positive net growth in the following productive summer season was observed. The trigger for the vertical positioning of filaments within the metalimnion was irradiance and not maximal water column stability. Repetitive disruptions of the vernal metalimnion owing to unstable weather conditions, as in spring 2019, went in parallel with a massive breakdown of the standing stock and marginal regrowth during thermal stratification. (iii) Driven by light intensity,P. rubescenswas entrained into the turbulent epilimnion in autumn, followed by a second peak in population growth. Thus, the typical bimodal growth pattern was still intact during the last decade. Our long-term study highlights the finely tuned interplay between climate-induced changes and variability of thermal stratification dynamics and physiological traits ofP. rubescens, determining its survival in a mesotrophic temperate lake.