Seasonal shifts in Fe-acquisition strategies in Southern Ocean microbial communities revealed by metagenomics and autonomous sampling

Iron (Fe) governs the cycling of organic carbon in large parts of the Southern Ocean. The strategies of diverse microbes to acquire the different chemical forms of Fe under seasonally changing organic carbon regimes remain, however, poorly understood. Here, we report high-resolution seasonal metagenomic observations from the region off Kerguelen Island (Indian Sector of the Southern Ocean) where natural Fe-fertilization induces consecutive spring and summer phytoplankton blooms. Our data illustrate pronounced, but distinct seasonal patterns in the abundance of genes implicated in the transport of different forms of Fe and organic substrates, of siderophore biosynthesis and carbohydrate-active enzymes. The seasonal dynamics suggest a temporal decoupling in the prokaryotic requirements of Fe and organic carbon during the spring phytoplankton bloom and a concerted access to these resources after the summer bloom. Taxonomic assignments revealed differences in the prokaryotic groups harbouring genes of a given Fe-related category and pronounced seasonal successions were observed. Using MAGs we could decipher the respective Fe- and organic substrate-related genes of individual taxa assigned to abundant groups. The ecological strategies related to Fe-acquisition provide insights on how this element could shape microbial community composition with potential implications on organic matter transformations in the Southern Ocean.     

Genomic mosaicism underlies the adaptation of marine Synechococcus ecotypes to distinct oceanic iron niches

Phytoplankton are limited by iron (Fe) in ~40% of the world's oceans including high-nutrient low-chlorophyll (HNLC) regions. While low-Fe adaptation has been well-studied in large eukaryotic diatoms, less is known for small, prokaryotic marine picocyanobacteria. This study reveals key physiological and genomic differences underlying Fe adaptation in marine picocyanobacteria. HNLC ecotype CRD1 strains have greater physiological tolerance to low Fe congruent with their expanded repertoire of Fe transporter, storage and regulatory genes compared to other ecotypes. From metagenomic analysis, genes encoding ferritin, flavodoxin, Fe transporters and siderophore uptake genes were more abundant in low-Fe waters, mirroring paradigms of low-Fe adaptation in diatoms. Distinct Fe-related gene repertories of HNLC ecotypes CRD1 and CRD2 also highlight how coexisting ecotypes have evolved independent approaches to life in low-Fe habitats. Synechococcus and Prochlorococcus HNLC ecotypes likewise exhibit independent, genome-wide reductions of predicted Fe-requiring genes. HNLC ecotype CRD1 interestingly was most similar to coastal ecotype I in Fe physiology and Fe-related gene content, suggesting populations from these different biomes experience similar Fe-selective conditions. This work supports an improved perspective that phytoplankton are shaped by more nuanced Fe niches in the oceans than previously implied from mostly binary comparisons of low- versus high-Fe habitats and populations.     

Diatoms shape the biogeography of heterotrophic prokaryotes in early spring in the Southern Ocean

The interplay among microorganisms profoundly impacts biogeochemical cycles in the ocean. Culture-based work has illustrated the diversity of diatom–prokaryote interactions, but the question of whether these associations can affect the spatial distribution of microbial communities is open. Here, we investigated the relationship between assemblages of diatoms and of heterotrophic prokaryotes in surface waters of the Indian sector of the Southern Ocean in early spring. The community composition of diatoms and that of total and active prokaryotes were different among the major ocean zones investigated. We found significant relationships between compositional changes of diatoms and of prokaryotes. In contrast, spatial changes in the prokaryotic community composition were not related to geographic distance and to environmental parameters when the effect of diatoms was accounted for. Diatoms explained 30% of the variance in both the total and the active prokaryotic community composition in early spring in the Southern Ocean. Using co-occurrence analyses, we identified a large number of highly significant correlations between abundant diatom species and prokaryotic taxa. Our results show that key diatom species of the Southern Ocean are each associated with a distinct prokaryotic community, suggesting that diatom assemblages contribute to shaping the habitat type for heterotrophic prokaryotes.     

Prokaryotic community dynamics and nitrogen-cycling genes in an oxygen-deficient upwelling system during La Niña and El Niño conditions

Dissolved oxygen regulates microbial distribution and nitrogen cycling and, therefore, ocean productivity and Earth's climate. To date, the assembly of microbial communities in relation to oceanographic changes due to El Niño Southern Oscillation (ENSO) remains poorly understood in oxygen minimum zones (OMZ). The Mexican Pacific upwelling system supports high productivity and a permanent OMZ. Here, the spatiotemporal distribution of the prokaryotic community and nitrogen-cycling genes was investigated along a repeated transect subjected to varying oceanographic conditions associated with La Niña in 2018 and El Niño in 2019. The community was more diverse during La Niña and in the aphotic OMZ, dominated by the Subtropical Subsurface water mass, where the highest abundances of nitrogen-cycling genes were found. The largest proportion of the Gulf of California water mass during El Niño provided warmer, more oxygenated, and nutrient-poor waters towards the coast, leading to a significant increase of Synechococcus in the euphotic layer compared with the opposite conditions during La Niña. These findings suggest that prokaryotic assemblages and nitrogen genes are linked to local physicochemical conditions (e.g. light, oxygen, nutrients), but also to oceanographic fluctuations associated with ENSO phases, indicating the crucial role of climate variability in microbial community dynamics in this OMZ.     

Seasonal dynamics of prokaryotes and their associations with diatoms in the Southern Ocean as revealed by an autonomous sampler

The Southern Ocean remains one of the least explored marine environments. The investigation of temporal microbial dynamics has thus far been hampered by the limited access to this remote ocean. We present here high-resolution seasonal observations of the prokaryotic community composition during phytoplankton blooms induced by natural iron fertilization. A total of 18 seawater samples were collected by a moored remote autonomous sampler over 4 months at 5–11 day intervals in offshore surface waters (central Kerguelen Plateau). Illumina sequencing of the 16S rRNA gene revealed that among the most abundant amplicon sequence variants, SAR92 and Aurantivirga were the first bloom responders, Pseudomonadaceae, Nitrincolaceae and Polaribacter had successive peaks during the spring bloom decline, and Amylibacter increased in relative abundance later in the season. SAR11 and SUP05 were abundant prior to and after the blooms. Using network analysis, we identified two groups of diatoms representative of the spring and summer bloom that had opposite correlation patterns with prokaryotic taxa. Our study provides the first seasonal picture of microbial community dynamics in the open Southern Ocean and thereby offers biological insights to the cycling of carbon and iron, and to an important puzzling issue that is the modest nitrate decrease associated to iron fertilization.     

Metabolic reprogramming by viruses in the sunlit and dark ocean

Background

Marine ecosystem function is largely determined by matter and energy transformations mediated by microbial community interaction networks. Viral infection modulates network properties through mortality, gene transfer and metabolic reprogramming.

Results

Here we explore the nature and extent of viral metabolic reprogramming throughout the Pacific Ocean depth continuum. We describe 35 marine viral gene families with potential to reprogram metabolic flux through central metabolic pathways recovered from Pacific Ocean waters. Four of these families have been previously reported but 31 are novel. These known and new carbon pathway auxiliary metabolic genes were recovered from a total of 22 viral metagenomes in which viral auxiliary metabolic genes were differentiated from low-level cellular DNA inputs based on small subunit ribosomal RNA gene content, taxonomy, fragment recruitment and genomic context information. Auxiliary metabolic gene distribution patterns reveal that marine viruses target overlapping, but relatively distinct pathways in sunlit and dark ocean waters to redirect host carbon flux towards energy production and viral genome replication under low nutrient, niche-differentiated conditions throughout the depth continuum.

Conclusions

Given half of ocean microbes are infected by viruses at any given time, these findings of broad viral metabolic reprogramming suggest the need for renewed consideration of viruses in global ocean carbon models.     

Linking Microbial Community Structure to S,N and Fe Biogeochemical Cycling in the Hot Springs at the Tengchong Geothermal Fields,Southwest China

Sediment and water samples collected from one acidic and three alkaline high temperature hot springs at the Tengchong terrestrial geothermal field, Southwest China, were examined using mineralogical, geochemical, and molecular biological techniques. The mineralogical and geochemical analyses suggested that these hot springs contained relatively high concentrations of S, Fe and N chemical species. Specifically, the acidic water was rich in Fe²⁺, SO₄^2? and NH₄⁺, while the alkaline waters were high in NO₃^?, H₂S and S₂O₃^?. Analyses of 16S rRNA gene sequences showed their bacterial communities were dominated by phyla Aquificae, Cyanobacteria, Deinococci-Thermus, Firmicutes, Proteobacteria, and Thermodesulfobacteria, while the archaeal clone libraries were dominated by orders Desulfurococcales, Sulfolobales, and Thermoproteales. Potential S-, N- and Fe-metabolizing prokaryotes were present at a relatively high proportion, but with large differences in the diversity and metabolic functions of each sample. These findings provide implications for uncovering microbial functions in elemental biogeochemical cycles within the Tengchong geothermal environments: i). the distinct differences in abundance and diversity of microbial communities in geothermal sediments were related to different in situ physicochemical conditions; ii). the S-, N- and Fe-related prokaryotes would take advantage of the strong chemical disequilibria in the hot springs; and iii). in return, their metabolic activities could promote the transformation of the S, Fe and N chemical species, thereby forming the basis of biogeochemical cycles in the terrestrial geothermal environments.     

Latitudinal distribution of prokaryotic picoplankton populations in the Atlantic Ocean

Members of the prokaryotic picoplankton are the main drivers of the biogeochemical cycles over large areas of the world's oceans. In order to ascertain changes in picoplankton composition in the euphotic and twilight zones at an ocean basin scale we determined the distribution of 11 marine bacterial and archaeal phyla in three different water layers along a transect across the Atlantic Ocean from South Africa (32.9°S) to the UK (46.4°N) during boreal spring. Depth profiles down to 500 m at 65 stations were analysed by catalysed reporter deposition fluorescence in situ hybridization (CARD‐FISH) and automated epifluorescence microscopy. There was no obvious overall difference in microbial community composition between the surface water layer and the deep chlorophyll maximum (DCM) layer. There were, however, significant differences between the two photic water layers and the mesopelagic zone. SAR11 (35 ± 9%) and Prochlorococcus (12 ± 8%) together dominated the surface waters, whereas SAR11 and Crenarchaeota of the marine group I formed equal proportions of the picoplankton community below the DCM (both ～15%). However, due to their small cell sizes Crenarchaeota contributed distinctly less to total microbial biomass than SAR11 in this mesopelagic water layer. Bacteria from the uncultured Chloroflexi‐related clade SAR202 occurred preferentially below the DCM (4–6%). Distinct latitudinal distribution patterns were found both in the photic zone and in the mesopelagic waters: in the photic zone, SAR11 was more abundant in the Northern Atlantic Ocean (up to 45%) than in the Southern Atlantic gyre (～25%), the biomass of Prochlorococcus peaked in the tropical Atlantic Ocean, and Bacteroidetes and Gammaproteobacteria bloomed in the nutrient‐rich northern temperate waters and in the Benguela upwelling. In mesopelagic waters, higher proportions of SAR202 were present in both central gyre regions, whereas Crenarchaeota were clearly more abundant in the upwelling regions and in higher latitudes. Other phylogenetic groups such as the Planctomycetes, marine group II Euryarchaeota and the uncultured clades SAR406, SAR324 and SAR86 rarely exceeded more than 5% of relative abundance.     

A metaproteomic assessment of winter and summer bacterioplankton from Antarctic Peninsula coastal surface waters

A metaproteomic survey of surface coastal waters near Palmer Station on the Antarctic Peninsula, West Antarctica, was performed, revealing marked differences in the functional capacity of summer and winter communities of bacterioplankton. Proteins from Flavobacteria were more abundant in the summer metaproteome, whereas winter was characterized by proteins from ammonia-oxidizing Marine Group I Crenarchaeota. Proteins prevalent in both seasons were from SAR11 and Rhodobacterales clades of Alphaproteobacteria, as well as many lineages of Gammaproteobacteria. The metaproteome data were used to elucidate the main metabolic and energy generation pathways and transport processes occurring at the microbial level in each season. In summer, autotrophic carbon assimilation appears to be driven by oxygenic photoautotrophy, consistent with high light availability and intensity. In contrast, during the dark polar winter, the metaproteome supported the occurrence of chemolithoautotrophy via the 3-hydroxypropionate/4-hydroxybutyrate cycle and the reverse tricarboxylic acid cycle of ammonia-oxidizing archaea and nitrite-oxidizing bacteria, respectively. Proteins involved in nitrification were also detected in the metaproteome. Taurine appears to be an important source of carbon and nitrogen for heterotrophs (especially SAR11), with transporters and enzymes for taurine uptake and degradation abundant in the metaproteome. Divergent heterotrophic strategies for Alphaproteobacteria and Flavobacteria were indicated by the metaproteome data, with Alphaproteobacteria capturing (by high-affinity transport) and processing labile solutes, and Flavobacteria expressing outer membrane receptors for particle adhesion to facilitate the exploitation of non-labile substrates. TonB-dependent receptors from Gammaproteobacteria and Flavobacteria (particularly in summer) were abundant, indicating that scavenging of substrates was likely an important strategy for these clades of Southern Ocean bacteria. This study provides the first insight into differences in functional processes occurring between summer and winter microbial communities in coastal Antarctic waters, and particularly highlights the important role that ‘dark'' carbon fixation has in winter.     

Distribution of Roseobacter RCA and SAR11 lineages and distinct bacterial communities from the subtropics to the Southern Ocean

We assessed the composition of the bacterioplankton in the Atlantic sector of the Southern Ocean in austral fall and winter and in New Zealand coastal waters in summer. The various water masses between the subtropics/Agulhas–Benguela boundary region and the Antarctic coastal current exhibited distinct bacterioplankton communities with the highest richness in the polar frontal region, as shown by denaturing gradient gel electrophoresis of 16S rRNA gene fragments. The SAR11 clade and the Roseobacter clade‐affiliated (RCA) cluster were quantified by real‐time quantitative PCR. SAR11 was detected in all samples analysed from subtropical waters to the coastal current and to depths of > 1000 m. In fall and winter, this clade constituted < 3% to 48% and 4–28% of total bacterial 16S rRNA genes respectively, with highest fractions in subtropical to polar frontal regions. The RCA cluster was only present in New Zealand coastal surface waters not exceeding 17°C, in the Agulhas–Benguela boundary region (visited only during the winter cruise), in subantarctic waters and in the Southern Ocean. In fall, this cluster constituted up to 36% of total bacterial 16S rRNA genes with highest fractions in the Antarctic coastal current and outnumbered the SAR11 clade at most stations in the polar frontal region and further south. In winter, the RCA cluster constituted lower proportions than the SAR11 clade and did not exceed 8% of total bacterial 16S rRNA genes. In fall, the RCA cluster exhibited significant positive correlations with latitude and ammonium concentrations and negative correlations with concentrations of nitrate, phosphate, and for near‐surface samples also with chlorophyll a, biomass production of heterotrophic prokaryotes and glucose turnover rates. The findings show that the various water masses between the subtropics and the Antarctic coastal current harbour distinct bacterioplankton communities. They further indicate that the RCA cluster, despite the narrow sequence similarity of > 98% of its 16S rRNA gene, is an abundant component of the heterotrophic bacterioplankton in the Southern Ocean, in particular in its coldest regions.     

The potential significance of microbial Fe(III) reduction during deposition of Precambrian banded iron formations

During deposition of late Archean–early Palaeoproterozoic Precambrian banded iron formations (BIFs) the downward flux of ferric hydroxide (Fe(OH)₃) and phytoplankton biomass should have facilitated microbial Fe(III) reduction. However, quantifying the significance of such a metabolic pathway in the Precambrian is extremely difficult, considering the post‐depositional alteration of the rocks and the lack of ideal modern analogues. Consequently, we have very few constraints on the Fe cycle at that time, namely (i) the concentration of dissolved Fe(II) in the ocean waters; (ii) by what mechanisms Fe(II) was oxidized (chemical, photochemical or biological, the latter using either O₂ or light); (iii) where the ferric hydroxide was precipitated (over the shelf vs. open ocean); (iv) the amount of phytoplankton biomass, which relates to the nutrient status of the surface waters; (v) the relative importance of Fe(III) reduction vs. the other types of metabolic pathways utilized by sea floor microbial communities; and (vi) the proportion of primary vs. diagenetic Fe(II) in BIF. Furthermore, although estimates can be made regarding the quantity of reducing equivalents necessary to account for the diagenetic Fe(II) component in Fe‐rich BIF layers, those same estimates do not offer any insights into the magnitude of Fe(III) actually generated within the water column, and hence, the efficiency of Fe and C recycling prior to burial. Accordingly, in this study, we have attempted to model the ancient Fe cycle, based simply on conservative experimental rates of photosynthetic Fe(II) oxidation in the euphotic zone. We estimate here that under ideal growth conditions, as much as 70% of the biologically formed Fe(III) could have been recycled back into the water column via fermentation and organic carbon oxidation coupled to microbial Fe(III) reduction. By comparing the potential amount of biomass generated phototrophically with the reducing equivalents required for Fe(III) reduction and magnetite formation, we also hypothesize that another anaerobic metabolic pathway might have been utilized in the surface sediment to oxidize the fermentation by‐products. Based on the premise that the deep ocean waters were anoxic, this role could have been fulfilled by methanogens, and maybe even methanotrophs that employed Fe(III) reduction.     

Changes in Bacterial and Archaeal Community Structure and Functional Diversity along a Geochemically Variable Soil Profile

Spatial heterogeneity in physical, chemical, and biological properties of soils allows for the proliferation of diverse microbial communities. Factors influencing the structuring of microbial communities, including availability of nutrients and water, pH, and soil texture, can vary considerably with soil depth and within soil aggregates. Here we investigated changes in the microbial and functional communities within soil aggregates obtained along a soil profile spanning the surface, vadose zone, and saturated soil environments. The composition and diversity of microbial communities and specific functional groups involved in key pathways in the geochemical cycling of nitrogen, Fe, and sulfur were characterized using a coupled approach involving cultivation-independent analysis of both 16S rRNA (bacterial and archaeal) and functional genes (amoA and dsrAB) as well as cultivation-based analysis of Fe(III)-reducing organisms. Here we found that the microbial communities and putative ammonia-oxidizing and Fe(III)-reducing communities varied greatly along the soil profile, likely reflecting differences in carbon availability, water content, and pH. In particular, the Crenarchaeota 16S rRNA sequences are largely unique to each horizon, sharing a distribution and diversity similar to those of the putative (amoA-based) ammonia-oxidizing archaeal community. Anaerobic microenvironments within soil aggregates also appear to allow for both anaerobic- and aerobic-based metabolisms, further highlighting the complexity and spatial heterogeneity impacting microbial community structure and metabolic potential within soils.     

Archaeal and bacterial communities of heavy metal contaminated acidic waters from zinc mine residues in Sepetiba Bay

Mining of metallic sulfide ore produces acidic water with high metal concentrations that have harmful consequences for aquatic life. To understand the composition and structure of microbial communities in acid mine drainage (AMD) waters associated with Zn mine tailings, molecular diversity of 16S genes was examined using a PCR, cloning, and sequencing approach. A total of 78 operational taxonomic units (OTUs) were obtained from samples collected at five different sites in and around mining residues in Sepetiba Bay, Brazil. We analyzed metal concentration, physical, chemical, and microbiological parameters related to prokaryotic diversity in low metal impacted compared to highly polluted environments with Zn at level of gram per liter and Cd–Pb at level of microgram per liter. Application of molecular methods for community structure analyses showed that Archaea and Bacteria groups present a phylogenetic relationship with uncultured environmental organisms. Phylogenetic analysis revealed that bacteria present at the five sites fell into seven known divisions, α-Proteobacteria (13.4%), β-Proteobacteria (16.3%), γ-Proteobacteria (4.3%), Sphingobacteriales (4.3%), Actinobacteria (3.2%) Acidobacteria (2.1%), Cyanobacteria (11.9%), and unclassified bacteria (44.5%). Almost all archaeal clones were related to uncultivated Crenarchaeota species, which were shared between high impacted and low impacted waters. Rarefaction curves showed that bacterial groups are more diverse than archaeal groups while the overall prokaryotic biodiversity is lower in high metal impacted environments than in less polluted habitats. Knowledge of this microbial community structure will help in understanding prokaryotic diversity, biogeography, and the role of microorganisms in zinc smelting AMD generation and perhaps it may be exploited for environmental remediation procedures in this area.     

New findings of <Emphasis Type="Italic">Lophius litulon</Emphasis> (Lophiidae) off the Southern Kurils

Data on new captures of juveniles of the yellow anglerfish Lophius litulon off the Southern Kurils are presented. Outer morphological characters of the specimens caught in waters off the Southern Kurils are described in comparison with those of specimens from other regions of the north-western part of the Pacific Ocean. Probable pathways of penetration of anglerfish (Lophiidae) to Russian Far East waters are discussed.     

Functional Potential of Soil Microbial Communities in the Maize Rhizosphere

Microbial communities in the rhizosphere make significant contributions to crop health and nutrient cycling. However, their ability to perform important biogeochemical processes remains uncharacterized. Here, we identified important functional genes that characterize the rhizosphere microbial community to understand metabolic capabilities in the maize rhizosphere using the GeoChip-based functional gene array method. Significant differences in functional gene structure were apparent between rhizosphere and bulk soil microbial communities. Approximately half of the detected gene families were significantly (p<0.05) increased in the rhizosphere. Based on the detected gyrB genes, Gammaproteobacteria, Betaproteobacteria, Firmicutes, Bacteroidetes and Cyanobacteria were most enriched in the rhizosphere compared to those in the bulk soil. The rhizosphere niche also supported greater functional diversity in catabolic pathways. The maize rhizosphere had significantly enriched genes involved in carbon fixation and degradation (especially for hemicelluloses, aromatics and lignin), nitrogen fixation, ammonification, denitrification, polyphosphate biosynthesis and degradation, sulfur reduction and oxidation. This research demonstrates that the maize rhizosphere is a hotspot of genes, mostly originating from dominant soil microbial groups such as Proteobacteria, providing functional capacity for the transformation of labile and recalcitrant organic C, N, P and S compounds.     

Microbial community development on model particles in the deep sulfidic waters of the Black Sea

Microorganisms attached to particles have been shown to be different from free-living microbes and to display diverse metabolic activities. However, little is known about the ecotypes associated with particles and their substrate preference in anoxic marine waters. Here, we investigate the microbial community colonizing particles in the anoxic and sulfide-rich waters of the Black Sea. We incubated beads coated with different substrates in situ at 1000 and 2000 m depth. After 6 h, the particle-attached microbes were dominated by Gamma- and Alpha-proteobacteria, and groups related to the phyla Latescibacteria, Bacteroidetes, Planctomycetes and Firmicutes, with substantial variation across the bead types, indicating that the attaching communities were selected by the substrate. Further laboratory incubations for 7 days suggested the presence of a community of highly specialized taxa. After incubation for 35 days, the microbial composition across all beads and depths was similar and primarily composed of putative sulfur cycling microbes. In addition to the major shared microbial groups, subdominant taxa on chitin and protein-coated beads were detected pointing to specialized microbial degraders. These results highlight the role of particles as sites for attachment and biofilm formation, while the composition of organic matter defined a secondary part of the microbial community.     

Plankton metabolism in the Greenland Sea during the polar summer of 2007

The polar summer metabolism of the planktonic communities in the Greenland Sea was surveyed in July 2007. Planktonic metabolism showed great variability across the studied area, with on average, higher metabolic rates in the Fram Strait-Svalbard region than along the Greenland Current. A significant fraction (47%) of the planktonic communities in the Fram Strait-Svalbard region were net heterotrophic, suggesting that increased respiration rates with further warming may lead the planktonic communities at this region to act as net CO₂ sources. The thresholds gross primary production for metabolic balance (i.e., gross primary production = community respiration) was much higher in the European sector of the Arctic than reported for the Southern Ocean, suggesting that heterotrophic metabolism is more prevalent in the European sector of the Arctic than in the Southern Ocean, indicating high allochthonous inputs in the Arctic region.