Interactions shape aquatic microbiome responses to Cu and Au nanoparticle treatments in wetland manipulation experiments.

In natural systems, organisms are embedded in complex networks where their physiology and community composition is shaped by both biotic and abiotic factors. Therefore, to assess the ecosystem-level effects of contaminants, we must pair complex, multi-trophic field studies with more targeted hypothesis-driven approaches to explore specific actors and mechanisms. Here, we examine aquatic microbiome responses to long-term additions of commercially-available metallic nanoparticles [copper-based (CuNPs) or gold (AuNPs)] and/or nutrients in complex, wetland mesocosms over 9 months, allowing for a full growth cycle of the aquatic plants. We found that both CuNPs and AuNPs (but not nutrient) treatments showed shifts in microbial communities and populations largely at the end of the experiment, as the aquatic plant community senesced. we examine aquatic microbiomes under chronic dosing of NPs and nutrients Simplified microbe-only or microbe + plant incubations revealed that direct effects of AuNPs on aquatic microbiomes can be buffered by plants (regardless of seasonal As mesocosms were dosed weekly, the absence of water column accumulation indicates the partitioning of both metals into other environmental compartments, mainly the floc and aquatic plants photosynthetically-derived organic matter. Overall, this study identifies the potential for NP environmental impacts to be either suppressed by or propagated across trophic levels via the presence of primary producers, highlighting the importance of organismal interactions in mediating emerging contaminants' ecosystem-wide impacts.

Host genotype structures the microbiome of a globally dispersed marine phytoplankton.

Phytoplankton support complex bacterial microbiomes that rely on phytoplankton-derived extracellular compounds and perform functions necessary for algal growth. Recent work has revealed sophisticated interactions and exchanges of molecules between specific phytoplankton-bacteria pairs, but the role of host genotype in regulating those interactions is unknown. Here, we show how phytoplankton microbiomes are shaped by intraspecific genetic variation in the host using global environmental isolates of the model phytoplankton host Thalassiosira rotula and a laboratory common garden experiment. A set of 81 environmental T. rotula genotypes from three ocean basins and eight genetically distinct populations did not reveal a core microbiome. While no single bacterial phylotype was shared across all genotypes, we found strong genotypic influence of T. rotula, with microbiomes associating more strongly with host genetic population than with environmental factors. The microbiome association with host genetic population persisted across different ocean basins, suggesting that microbiomes may be associated with host populations for decades. To isolate the impact of host genotype on microbiomes, a common garden experiment using eight genotypes from three distinct host populations again found that host genotype influenced microbial community composition, suggesting that a process we describe as genotypic filtering, analogous to environmental filtering, shapes phytoplankton microbiomes. In both the environmental and laboratory studies, microbiome variation between genotypes suggests that other factors influenced microbiome composition but did not swamp the dominant signal of host genetic background. The long-term association of microbiomes with specific host genotypes reveals a possible mechanism explaining the evolution and maintenance of complex phytoplankton-bacteria chemical exchanges.

Vertical community patterns of Labyrinthulomycetes protists reveal their potential importance in the oceanic biological pump.

The biological pump plays a vital role in exporting organic particles into the deep ocean for long-term carbon sequestration. However, much remains unknown about some of its key microbial players. In this study, Labyrinthulomycetes protists (LP) were used to understand the significance of heterotrophic microeukaryotes in the transport of particulate organic matter from the surface to the dark ocean. Unlike the sharp vertical decrease of prokaryotic biomass, the LP biomass only slightly decreased with depth and eventually exceeded prokaryotic biomass in the bathypelagic layer. Sequencing identified high diversity of the LP communities with a dominance of Aplanochytrium at all depths. Notably, ASVs that were observed in the surface layer comprised ~20% of ASVs and ~60% of sequences in each of the deeper (including bathypelagic) layers, suggesting potential vertical export of the LP populations to the deep ocean. Further analyses of the vertical patterns of the 50 most abundant ASVs revealed niche partitioning of LP phylotypes in the pelagic ocean, including those that could decompose organic detritus and/or facilitate the formation of fast-sinking particles. Overall, this study presents several lines of evidence that the LP can be an important component of the biological pump through their multiple ecotypes in the pelagic ocean.

Rapid changes in coastal ocean microbiomes uncoupled with shifts in environmental variables.

Disturbances, here defined as events that directly alter microbial community composition, are commonly studied in host-associated and engineered systems. In spite of global change both altering environmental averages and increasing extreme events, there has been relatively little research into the causes, persistence and population-level impacts of disturbance in the dynamic coastal ocean. Here, we utilize 3 years of observations from a coastal time series to identify disturbances based on the largest week-over-week changes in the microbiome (i.e. identifying disturbance as events that alter the community composition). In general, these microbiome disturbances were not clearly linked to specific environmental factors and responsive taxa largely differed, aside from SAR11, which generally declined. However, several disturbance metagenomes identified increased phage-associated genes, suggesting that unexplained community shifts might be caused by increased mortality. Furthermore, a category 1 hurricane, the only event that would likely be classified a priori as an environmental disturbance, was not an outlier in microbiome composition, but did enhance a bloom in seasonally abundant phytoplankton. Thus, as extreme environmental changes intensify, assumptions of what constitutes a disturbance should be re-examined in the context of ecological history and microbiome responses.

Annual Partitioning Patterns of Labyrinthulomycetes Protists Reveal Their Multifaceted Role in Marine Microbial Food Webs.

Heterotrophic microbes play a key role in remineralizing organic material in the coastal ocean. While there is a significant body of literature examining heterotrophic bacterioplankton and phytoplankton communities, much less is known about the diversity, dynamics, and ecology of eukaryotic heterotrophs. Here, we focus on the Labyrinthulomycetes, a fungus-like protistan group whose biomass can exceed that of the bacterioplankton in coastal waters. We examined their diversity and community structure in a weekly temperate coastal ocean time series. Their seasonal community patterns were related to temperature, insolation, dissolved inorganic carbon, fungal abundance, ammonia, chlorophyll a, pH, and other environmental variables. Similar to the bacterioplankton, annual community patterns of the Labyrinthulomycetes were dominated by a few persistent taxa with summer or winter preferences. However, like the patterns of fungi at this site, the majority of the Labyrinthulomycetes phylotypes occurred mostly as short, reoccurring, season-specific blooms. Furthermore, some specific phylotypes of Labyrinthulomycetes displayed time-lagged correlations or cooccurrences with bacterial, algal, or fungal phylotypes, suggesting their potentially multifaceted involvement in the marine food webs. Overall, this study reports niche partitioning between closely related Labyrinthulomycetes and identifies distinct ecotypes and temporal patterns compared to bacterioplankton and fungi.IMPORTANCE Increasing evidence has shown that heterotrophic microeukaryotes are an important component in global marine ecosystems, while their diversity and ecological functions remain largely unknown. Without appropriately incorporating these organisms into the food web models, our current understanding of marine microbial community ecology is incomplete, which may further hamper broader studies of biogeochemistry and climate change. This study focuses on a major group of unicellular fungus-like protists (Labyrinthulomycetes) and reveals their distinct annual community patterns relative to fungi and bacteria. Results of our observations provide new information on the community structure and ecology of this protistan group and shed light on the intricate ecological roles of unicellular heterotrophic eukaryotes in the coastal oceans.

Microbial communities across nearshore to offshore coastal transects are primarily shaped by distance and temperature.

Recent studies have focused on linking marine microbial communities with environmental factors, yet, relatively little is known about the drivers of microbial community patterns across the complex gradients from the nearshore to open ocean. Here, we examine microbial dynamics in 15 five-station transects beginning at the estuarine Piver's Island Coastal Observatory (PICO) time-series site and continuing 87 km across the continental shelf to the oligotrophic waters of the Sargasso Sea. 16S rRNA gene libraries reveal strong clustering by sampling site with distinct nearshore, continental shelf and offshore oceanic communities. Water temperature and distance from shore (which serves as a proxy for gradients in factors such as productivity, terrestrial input and nutrients) both most influence community composition. However, at the phylotype level, modelling shows the distribution of some taxa is linked to temperature, others to distance from shore and some by both factors, highlighting that taxa with distinct environmental preferences underlie apparent clustering by station. Thus, continental margins contain microbial communities that are distinct from those of either the nearshore or the offshore environments and contain mixtures of phylotypes with nearshore or offshore preferences rather than those unique to the shelf environment.

Conserved Microbial Toxicity Responses for Acute and Chronic Silver Nanoparticle Treatments in Wetland Mesocosms.

Most studies of bacterial exposure to environmental contaminants focus on acute treatments; however, the impacts of single, high-dose exposures on microbial communities may not readily be extended to the more likely scenario of chronic, low-dose contaminant exposures. Here, in a year-long, wetland mesocosm experiment, we compared microbial community responses to pulse (single 450 mg dose of silver) and chronic (weekly 8.7 mg doses of silver for 1 year) silver nanoparticle (Ag0 NP) treatments, as well as a chronic treatment of "aged" sulfidized silver nanoparticles (Ag2S NPs). While mesocosms exposed to Ag2S NPs never differed significantly from the controls, both Ag0 NP treatments exhibited reduced microbial diversity and altered community composition; however, the effects differed in timing, duration, and magnitude. Microbial community-level impacts in the acute Ag0 NP treatment were apparent only within the first weeks and then converged on the control mesocosm composition, while chronic exposure effects were observed several months after exposures began, likely due to interactive effects of nanoparticle toxicity and winter environmental conditions. Notably, there was a high level of overlap in the taxa which exhibited significant declines (>10×) in both treatments, suggesting a conserved toxicity response for both pulse and chronic exposures. Thus, this research suggests that complex, but short-term, acute toxicological studies may provide critical, cost-effective insights into identifying microbial taxa sensitive to long-term chronic exposures to Ag NPs.

A High-Resolution Time Series Reveals Distinct Seasonal Patterns of Planktonic Fungi at a Temperate Coastal Ocean Site (Beaufort, North Carolina, USA).

There is a growing awareness of the ecological and biogeochemical importance of fungi in coastal marine systems. While highly diverse fungi have been discovered in these marine systems, still, little is known about their seasonality and associated drivers in coastal waters. Here, we examined fungal communities over 3 years of weekly sampling at a dynamic, temperate coastal site (Pivers Island Coastal Observatory [PICO], Beaufort, NC, USA). Fungal 18S rRNA gene abundance, operational taxonomic unit (OTU) richness, and Shannon's diversity index values exhibited prominent seasonality. Fungal 18S rRNA gene copies peaked in abundance during the summer and fall, with positive correlations with chlorophyll a, SiO4, and oxygen saturation. Diversity (measured using internal transcribed spacer [ITS] libraries) was highest during winter and lowest during summer; it was linked to temperature, pH, chlorophyll a, insolation, salinity, and dissolved inorganic carbon (DIC). Fungal communities derived from ITS libraries were dominated throughout the year by Ascomycota, with contributions from Basidiomycota, Chytridiomycota, and Mucoromycotina, and their seasonal patterns linked to water temperature, light, and the carbonate system. Network analysis revealed that while cooccurrence and exclusion existed within fungus networks, exclusion dominated the fungus-and-phytoplankton network, in contrast with reported pathogenic and nutritional interactions between marine phytoplankton and fungi. Compared with the seasonality of bacterial communities in the same samples, the timing, extent, and associated environmental variables for fungi community are unique. These results highlight the fungal seasonal dynamics in coastal water and improve our understanding of the ecology of planktonic fungi.IMPORTANCE Coastal fungal dynamics were long assumed to be due to terrestrial inputs; here, a high-resolution time series reveals strong, repeating annual patterns linked to in situ environmental conditions, arguing for a resident coastal fungal community shaped by environmental factors. These seasonal patterns do, however, differ from those observed in the bacterioplankton at the same site; e.g., fungal diversity peaks in winter, whereas bacterial diversity maxima occur in the spring and fall. While the dynamics of these communities are linked to water temperature and insolation, fungi are also influenced by the carbonate system (pH and DIC). As both fungi and heterotrophic bacteria are thought to be key organic-material metabolizers, differences in their environmental drivers may offer clues as to which group dominates secondary production at this dynamic site. Overall, this study suggests the unique ecological roles of mycoplankton and their potentially broad niche complementarities to other microbial groups in the coastal ocean.

Insensitivity of Diverse and Temporally Variable Particle-Associated Microbial Communities to Bulk Seawater Environmental Parameters.

UNLABELLED: There is a growing recognition of the roles of marine microenvironments as reservoirs of biodiversity and as sites of enhanced biological activity and in facilitating biological interactions. Here, we examine the bacterial community inhabiting free-living and particle-associated seawater microenvironments at the Pivers Island Coastal Observatory (PICO). 16S rRNA gene libraries from monthly samples (July 2013 to August 2014) were used to identify microbes in seawater in four size fractions: >63 µm (zooplankton and large particles), 63 to 5 µm (particles), 5 to 1 µm (small particles/dividing cells), and <1 µm (free-living prokaryotes). Analyses of microbial community composition highlight the importance of the microhabitat (e.g., particle-associated versus free-living lifestyle) as communities cluster by size fraction, and the microhabitat explains more of the community variability than measured environmental parameters, including pH, particle concentration, projected daily insolation, nutrients, and temperature. While temperature is statistically associated with community changes in the <1-µm and 5- to 1-µm fractions, none of the measured bulk seawater environmental variables are statistically significant in the larger-particle-associated fractions. These results, combined with high particle-associated community variability, especially in the largest size fraction (i.e., >63 µm), suggest that particle composition, including eukaryotes and their associated microbiomes, may be an important factor in selecting for specific particle-associated bacteria. IMPORTANCE: By comparing levels of particle-associated and free-living bacterial diversity at a coastal location over the course of 14 months, we show that bacteria associated with particles are generally more diverse and appear to be less responsive to commonly measured environmental variables than free-living bacteria. These diverse and highly variable particle-associated communities are likely driven by differences in particle substrates both within the water column at a single time point and due to seasonal changes over the course of the year.

Thermally adaptive tradeoffs in closely related marine bacterial strains.

Time series studies have shown that some bacterial taxa occur only at specific times of the year while others are ubiquitous in spite of seasonal shifts in environmental variables. Here, we ask if these ubiquitous clades are generalists that grow over a wide range of environmental conditions, or clusters of strain-level environmental specialists. To answer this question, vibrio strains isolated at a coastal time series were phylogenetically and physiologically characterized revealing three dominant strategies within the vibrio: mesophiles, psychrophiles and apparently generalist broad thermal range clades. Thermal performance curves from laboratory growth rate experiments help explain field observations of relative abundances: the mesophilic clade grows optimally at temperatures 16°C higher than the psychrophilic clade. Strains in the broad thermal range clade all have similar optimal growth temperatures but also exhibit temperature-related tradeoffs with faster growth rates for warm temperature strains and broader growth ranges for strains from cool temperatures. Moreover, the mechanisms of thermal adaptation apparently differ based on evolutionary time scales: shifts in the temperature of maximal growth occur between deeply branching clades but thermal performance curve shape changes on shorter time scales. Thus, apparently ubiquitous clades are likely not generalists, but contain subclusters with distinct environmental preferences.

Vibrio metoecus sp. nov., a close relative of Vibrio cholerae isolated from coastal brackish ponds and clinical specimens.

A Gram-staining-negative, curved-rod-shaped bacterium with close resemblance to Vibrio cholerae, the aetiological agent of cholera, was isolated over the course of several years from coastal brackish water (17 strains) and from clinical cases (two strains) in the United States. 16S rRNA gene identity with V. cholerae exceeded 98 % yet an average nucleotide identity based on genome data of around 86 % and multi locus sequence analysis of six housekeeping genes (mdh, adk, gyrB, recA, pgi and rpoB) clearly delineated these isolates as a distinct genotypic cluster within the V. cholerae-V. mimicus clade. Most standard identification techniques do not differentiate this cluster of isolates from V. cholerae. Only amplification of the ompW gene using V. cholerae-specific primers and a negative Voges-Proskauer test showed a difference between the two clusters. Additionally, all isolated strains differed phenotypically from V. cholerae in their ability to utilize N-acetyl-d-galactosamine and d-glucuronic acid as sole carbon sources. Furthermore, they were generally unable to infect the slime mould Dictyostelium discoideum, a widespread ability in V. cholerae. Based on these clear phenotypic differences that are not necessarily apparent in standard tests as well as average nucleotide identity and phylogeny of protein-coding genes, we propose the existence of a novel species, Vibrio metoecus sp. nov. with the type strain OP3H(T) ( = LMG 27764(T) = CIP 110643(T)). Due to its close resemblance to V. cholerae and the increasing number of strains isolated over the past several years, we suggest that V. metoecus sp. nov. is a relatively common species of the genus Vibrio, isolates of which have been identified as atypical isolates of V. cholerae in the past. Its isolation from clinical samples also indicates that strains of this species, like V. cholerae, are opportunistic pathogens.

Emerging contaminant or an old toxin in disguise? Silver nanoparticle impacts on ecosystems.

The use of antimicrobial silver nanoparticles (AgNPs) in consumer-products is rising. Much of these AgNPs are expected to enter the wastewater stream, with up to 10% of that eventually released as effluent into aquatic ecosystems with unknown ecological consequences. We examined AgNP impacts on aquatic ecosystems by comparing the effects of two AgNP sizes (12 and 49 nm) to ionic silver (Ag(+); added as AgNO3), a historically problematic contaminant with known impacts. Using 19 wetland mesocosms, we added Ag to the 360 L aquatic compartment to reach 2.5 mg Ag L(-1). Silver treatments and two coating controls were done in triplicate, and compared to four replicate controls. All three silver treatments were toxic to aquatic plants, leading to a significant release of dissolved organic carbon and chloride following exposure. Simultaneously, dissolved methane concentrations increased forty-fold relative to controls in all three Ag treatments. Despite dramatic toxicity differences observed in lab studies for these three forms of Ag, our results show surprising convergence in the direction, magnitude, and duration of ecosystem-scale impacts for all Ag treatments. Our results suggest that all forms of Ag changed solute chemistry driving transformations of Ag which then altered Ag impacts.

Oxygen levels differentially attenuate the structure and diversity of microbial communities in the oceanic oxygen minimal zones.

Global change mediated shifts in ocean temperature and circulation patterns, compounded by human activities, are leading to the expansion of marine oxygen minimum zones (OMZs) with concomitant alterations in nutrient and climate-active trace gas cycling. While many studies have reported distinct bacterial communities within OMZs, much of this research compares across depths rather with oxygen status and does not include eukayrotic microbes. Here, we investigated the Bay of Bengal (BoB) OMZ, where low oxygen conditions are persistent, but trace levels of oxygen remain (< 20 µM from 200 to 500 m). As other environmental variables are similar between OMZ and non-OMZ (NOZ) stations, we compared the abundance, diversity, and community composition of several microbial groups (bacterioplankton, Labyrinthulomycetes, and fungi) across oxygen levels. While prokaryote abundance decreased with depth, no significant differences existed across oxygen groups. In contrast, Labyrinthulomycetes abundance was significantly higher in non-OMZ stations but did not change significantly with depth, while fungal abundance was patchy without clear depth or oxygen-related trends. Bacterial and fungal diversity was lower in OMZ stations at 500 m, while Labyrinthulomycetes diversity only showed a depth-related profile, decreasing below the euphotic zone. Surprisingly, previously reported OMZ-associated bacterial taxa were not significantly more abundant at OMZ stations. Furthermore, compared to the bacterioplankton, fewer Labyrinthulomycetes and fungi taxa showed responses to oxygen status. Thus, this research identifies stronger oxygen-level linkages within the bacterioplankton than in the examined microeukaryotes.

Relationship between abundance and specific activity of bacterioplankton in open ocean surface waters.

Marine microbial communities are complex and dynamic, and their ecology impacts biogeochemical cycles in pelagic ecosystems. Yet, little is known about the relative activities of different microbial populations within genetically diverse communities. We used rRNA as a proxy for activity to quantify the relative specific activities (rRNA/ribosomal DNA [rDNA or rRNA genes]) of the eubacterial populations and to identify locations or clades for which there are uncouplings between specific activity and abundance. After analyzing 1.6 million sequences from 16S rDNA and rRNA (cDNA) libraries from two euphotic depths from a representative site in the Pacific Ocean, we show that although there is an overall positive relationship between the abundances (rDNAs) and activities (rRNAs) among populations of the bacterial community, for some populations these measures are uncoupled. Different ecological strategies are exemplified by the two numerically dominant clades at this site: the cyanobacterium Prochlorococcus is abundant but disproportionately more active, while the heterotrophic SAR11 is abundant but less active. Other rare populations, such as Alteromonas, have high specific activities in spite of their low abundances, suggesting intense population regulation. More detailed analyses using a complementary quantitative PCR (qPCR)-based approach of measuring relative specific activity for Prochlorococcus populations in the Pacific and Atlantic Oceans also show that specific activity, but not abundance, reflects the key drivers of light and nutrients in this system; our results also suggest substantial top-down regulation (e.g., grazing, viruses, or organismal interactions) or transport (e.g., mixing, immigration, or emigration) of these populations. Thus, we show here that abundance and specific activity can be uncoupled in open ocean systems and that describing both is critical to characterizing microbial communities and predicting marine ecosystem functioning and responses to change.

A Gulf Stream frontal eddy harbors a distinct microbiome compared to adjacent waters.

Mesoscale oceanographic features, including eddies, have the potential to alter productivity and other biogeochemical rates in the ocean. Here, we examine the microbiome of a cyclonic, Gulf Stream frontal eddy, with a distinct origin and environmental parameters compared to surrounding waters, in order to better understand the processes dominating microbial community assembly in the dynamic coastal ocean. Our microbiome-based approach identified the eddy as distinct from the surround Gulf Stream waters. The eddy-associated microbial community occupied a larger area than identified by temperature and salinity alone, increasing the predicted extent of eddy-associated biogeochemical processes. While the eddy formed on the continental shelf, after two weeks both environmental parameters and microbiome composition of the eddy were most similar to the Gulf Stream, suggesting the effect of environmental filtering on community assembly or physical mixing with adjacent Gulf Stream waters. In spite of the potential for eddy-driven upwelling to introduce nutrients and stimulate primary production, eddy surface waters exhibit lower chlorophyll a along with a distinct and less even microbial community, compared to the Gulf Stream. At the population level, the eddy microbiome exhibited differences among the cyanobacteria (e.g. lower Trichodesmium and higher Prochlorococcus) and in the heterotrophic alpha Proteobacteria (e.g. lower relative abundances of specific SAR11 phylotypes) versus the Gulf Stream. However, better delineation of the relative roles of processes driving eddy community assembly will likely require following the eddy and surrounding waters since inception. Additionally, sampling throughout the water column could better clarify the contribution of these mesoscale features to primary production and carbon export in the oceans.

Niche Partitioning of Labyrinthulomycete Protists Across Sharp Coastal Gradients and Their Putative Relationships With Bacteria and Fungi.

While planktonic microbes play key roles in the coastal oceans, our understanding of heterotrophic microeukaryotes' ecology, particularly their spatiotemporal patterns, drivers, and functions, remains incomplete. In this study, we focus on a ubiquitous marine fungus-like protistan group, the Labyrinthulomycetes, whose biomass can exceed that of bacterioplankton in coastal oceans but whose ecology is largely unknown. Using quantitative PCR and amplicon sequencing of their 18S rRNA genes, we examine their community variation in repeated five-station transects across the nearshore-to-offshore surface waters of North Carolina, United States. Their total 18S rRNA gene abundance and phylotype richness decrease significantly from the resource-rich nearshore to the oligotrophic offshore waters, but their Pielou's community evenness appears to increase offshore. Similar to the bacteria and fungi, the Labyrinthulomycete communities are significantly structured by distance from shore, water temperature, and other environmental factors, suggesting potential niche partitioning. Nevertheless, only several Labyrinthulomycete phylotypes, which belong to aplanochytrids, thraustochytrids, or unclassified Labyrinthulomycetes, are prevalent and correlated with cohesive bacterial communities, while more phylotypes are patchy and often co-occur with fungi. Overall, these results complement previous time-series observations that resolve the Labyrinthulomycetes as persistent and short-blooming ecotypes with distinct seasonal preferences, further revealing their partitioning spatial patterns and multifaceted roles in coastal marine microbial food webs.

Patchy Blooms and Multifarious Ecotypes of Labyrinthulomycetes Protists and Their Implication in Vertical Carbon Export in the Pelagic Eastern Indian Ocean.

Labyrinthulomycetes protists are an important heterotrophic component of microeukaryotes in the world's oceans, but their distribution patterns and ecological roles are poorly understood in pelagic waters. This study employed flow cytometry and high-throughput sequencing to characterize the abundance, diversity, and community structure of Labyrinthulomycetes in the pelagic Eastern Indian Ocean. The total Labyrinthulomycetes abundance varied much more among stations than did the abundance of prokaryotic plankton, reaching over 1,000 cells mL-1 at a few "bloom" stations. The total Labyrinthulomycetes abundance did not decline with depth throughout the whole water column (5 to 2,000 m) like the abundance of prokaryotic plankton did, and the Labyrinthulomycetes average projected biomass over all samples was higher than that of the prokaryotic plankton. However, Labyrinthulomycetes diversity showed obvious vertical variations, with richness, Shannon diversity, and evenness greatest in the upper epipelagic, lower epipelagic, and deep waters, respectively. Many abundant phylotypes were detected across multiple water layers, which aligned with the constant vertical Labyrinthulomycetes biomass, suggesting potential sinking and contribution to the biological pump. Hierarchical clustering revealed distinct ecotypes partitioning by vertical distribution patterns, suggesting their differential roles in the carbon cycle and storage processes. Particularly, most phylotypes showed patchy distributions (occurring in only few samples) as previously found in the coastal waters, but they were less associated with the Labyrinthulomycetes blooms than the prevalent phylotypes. Overall, this study revealed distinct patterns of Labyrinthulomycetes ecotypes and shed light on their importance in the pelagic ocean carbon cycling and sequestration relative to that of the prokaryotic plankton. IMPORTANCE While prokaryotic heterotrophic plankton are well accepted as major players in oceanic carbon cycling, the ecological distributions and functions of their microeukaryotic counterparts in the pelagic ocean remain largely unknown. This study focused on an important group of heterotrophic (mainly osmotrophic) protistan microbes, the Labyrinthulomycetes, whose biomass can surpass that of the prokaryotic plankton in many marine ecosystems, including the bathypelagic ocean. We found patchy horizontal but persistent vertical abundance profiles of the Labyrinthulomycetes protists in the pelagic waters of the Eastern Indian Ocean, which were distinct from the spatial patterns of the prokaryotic plankton. Moreover, multiple Labyrinthulomycetes ecotypes with distinct vertical patterns were detected and, based on the physiologic, metabolic, and genomic understanding of their cultivated relatives, were inferred to play multifaceted key roles in the carbon cycle and sequestration, particularly as contributors to the vertical carbon export from the surface to the dark ocean, i.e., the biological pump.

Rapid chemotactic response enables marine bacteria to exploit ephemeral microscale nutrient patches.

Because ocean water is typically resource-poor, bacteria may gain significant growth advantages if they can exploit the ephemeral nutrient patches originating from numerous, small sources. Although this interaction has been proposed to enhance biogeochemical transformation rates in the ocean, it remains questionable whether bacteria are able to efficiently use patches before physical mechanisms dissipate them. Here we show that the rapid chemotactic response of the marine bacterium Pseudoalteromonas haloplanktis substantially enhances its ability to exploit nutrient patches before they dissipate. We investigated two types of patches important in the ocean: nutrient pulses and nutrient plumes, generated for example from lysed algae and sinking organic particles, respectively. We used microfluidic devices to create patches with environmentally realistic dimensions and dynamics. The accumulation of P. haloplanktis in response to a nutrient pulse led to formation of bacterial hot spots within tens of seconds, resulting in a 10-fold higher nutrient exposure for the fastest 20% of the population compared with nonmotile cells. Moreover, the chemotactic response of P. haloplanktis was >10 times faster than the classic chemotaxis model Escherichia coli, leading to twice the nutrient exposure. We demonstrate that such rapid response allows P. haloplanktis to colonize nutrient plumes for realistic particle sinking speeds, with up to a 4-fold nutrient exposure compared with nonmotile cells. These results suggest that chemotactic swimming strategies of marine bacteria in patchy nutrient seascapes exert strong influence on carbon turnover rates by triggering the formation of microscale hot spots of bacterial productivity.

Patchy Distributions and Distinct Niche Partitioning of Mycoplankton Populations across a Nearshore to Open Ocean Gradient.

Evidence increasingly suggests planktonic fungi (or mycoplankton) play an important role in marine food webs and biogeochemical cycles. In order to better understand their ecological role and how oceanographic gradients from the coastal to open ocean shape the mycoplankton community, molecular approaches were used to study fungal dynamics along a repeatedly sampled, five-station transect beginning at the mouth of an estuary and continuing 87 km across the continental shelf to the oligotrophic waters at the boundary of the Sargasso Sea. Similar to patterns in chlorophyll a, fungal 18S rRNA gene abundance showed a sharp decrease from nearshore to offshore stations. While Shannon's diversity was not statistically different across the transect, nonmetric multidimensional scaling (NMDS) ordination revealed that fungal communities at the nearshore station were significantly different from those at other stations. Even though spatial gradients were consistently strong, the shelf mycoplankton were more similar to those of the offshore communities when temperature was high (>20°C) and while they shifted toward the nearshore communities when temperature was low (<19°C), suggesting a role for additional seasonal factors (such as temperature) in shaping mycoplankton distributions. However, overall phylotype distributions were patchy with few taxa observed at all stations and the majority observed at a single station with the nearshore station exhibiting the largest number of exclusive phylotypes. Overall, our findings revealed the patchy spatial distributions and distinct niche partitioning of mycoplankton populations across a nearshore to open ocean gradient, which improved our understanding of fungal ecology in coastal waters. IMPORTANCE Fungi are an important, but understudied, group of heterotrophic microbes in marine environments. Traditionally, fungi in the coastal ocean were largely assumed to be derived from terrestrial inputs. Yet here we find many fungal taxa are endemic to the open ocean environment but are rare or absent in nearshore waters, suggesting they are not washed into the ocean from the land. As observed for the bacterioplankton, coastal oceanographic gradients can function as habitat barriers to partition fungal communities. Compared to the bacterioplankton, however, the mycoplankton exhibit a much patchier distribution pattern, suggesting differential drivers and the potential for spatially/temporally limited habitats or strong density-dependent selection. Therefore, our results show that mycoplankton in the coastal ocean may play a significant but complementary role to that of the bacterioplankton.

Environmental stability impacts the differential sensitivity of marine microbiomes to increases in temperature and acidity.

Ambient conditions shape microbiome responses to both short- and long-duration environment changes through processes including physiological acclimation, compositional shifts, and evolution. Thus, we predict that microbial communities inhabiting locations with larger diel, episodic, and annual variability in temperature and pH should be less sensitive to shifts in these climate-change factors. To test this hypothesis, we compared responses of surface ocean microbes from more variable (nearshore) and more constant (offshore) sites to short-term factorial warming (+3 °C) and/or acidification (pH -0.3). In all cases, warming alone significantly altered microbial community composition, while acidification had a minor influence. Compared with nearshore microbes, warmed offshore microbiomes exhibited larger changes in community composition, phylotype abundances, respiration rates, and metatranscriptomes, suggesting increased sensitivity of microbes from the less-variable environment. Moreover, while warming increased respiration rates, offshore metatranscriptomes yielded evidence of thermal stress responses in protein synthesis, heat shock proteins, and regulation. Future oceans with warmer waters may enhance overall metabolic and biogeochemical rates, but they will host altered microbial communities, especially in relatively thermally stable regions of the oceans.