Ecological differentiation between strains of bacterial species is shaped by genomic and metabolic variability. However, connecting genotypes to ecological niches remains a major challenge. Here, we linked bacterial geno- and phenotypes by contextualizing pangenomic, exometabolomic and physiological evidence in twelve strains of the marine bacterium Alteromonas macleodii, illuminating adaptive strategies of carbon metabolism, microbial interactions, cellular communication and iron acquisition. In A. macleodii strain MIT1002, secretion of amino acids and the unique capacity for phenol degradation may promote associations with Prochlorococcus cyanobacteria. Strain 83-1 and three novel Pacific isolates, featuring clonal genomes despite originating from distant locations, have profound abilities for algal polysaccharide utilization but without detrimental implications for Ecklonia macroalgae. Degradation of toluene and xylene, mediated via a plasmid syntenic to terrestrial Pseudomonas, was unique to strain EZ55. Benzoate degradation by strain EC673 related to a chromosomal gene cluster shared with the plasmid of A. mediterranea EC615, underlining that mobile genetic elements drive adaptations. Furthermore, we revealed strain-specific production of siderophores and homoserine lactones, with implications for nutrient acquisition and cellular communication. Phenotypic variability corresponded to different competitiveness in co-culture and geographic distribution, indicating linkages between intraspecific diversity, microbial interactions and biogeography. The finding of "ecological microdiversity" helps understanding the widespread occurrence of A. macleodii and contributes to the interpretation of bacterial niche specialization, population ecology and biogeochemical roles.
Abstract Submesoscale eddies and fronts are important components of oceanic mixing and energy fluxes. These phenomena occur in the surface ocean for a period of several days, on scales between a few hundred meters and few tens of kilometers. Remote sensing and modeling suggest that eddies and fronts may influence marine ecosystem dynamics, but their limited temporal and spatial scales make them challenging for observation and in situ sampling. Here, the study of a submesoscale filament in summerly Arctic waters (depth 0–400 m) revealed enhanced mixing of Polar and Atlantic water masses, resulting in a ca. 4 km wide and ca. 50 km long filament with distinct physical and biogeochemical characteristics. Compared to the surrounding waters, the filament was characterized by a distinct phytoplankton bloom, associated with depleted inorganic nutrients, elevated chlorophyll a concentrations, as well as twofold higher phyto‐ and bacterioplankton cell abundances. High‐throughput 16S rRNA gene sequencing of bacterioplankton communities revealed enrichment of typical phytoplankton bloom‐associated taxonomic groups (e.g., Flavobacteriales ) inside the filament. Furthermore, linked to the strong water subduction, the vertical export of organic matter to 400 m depth inside the filament was twofold higher compared to the surrounding waters. Altogether, our results show that physical submesoscale mixing can shape distinct biogeochemical conditions and microbial communities within a few kilometers of the ocean. Hence, the role of submesoscale features in polar waters for surface ocean biodiversity and biogeochemical processes need further investigation, especially with regard to the fate of sea ice in the warming Arctic Ocean.
We introduce the Global rRNA Universal Metabarcoding Plankton database (GRUMP), which consists of 1194 samples that were collected from 2003-2020 and cover extensive latitudinal and longitudinal transects, as well as depth profiles in all major ocean basins. DNA from unfractionated (> 0.2um) seawater samples was amplified using the 515Y/926R universal three-domain rRNA gene primers, simultaneously quantifying the relative abundance of amplicon sequencing variants (ASVs) from bacteria, archaea, eukaryotic nuclear 18S, and eukaryotic plastid 16S. Thus, the ratio between taxa in one sample is directly comparable to the ratio in any other GRUMP sample, regardless of gene copy number differences. This obviates a problem in prior global studies that used size-fractionation and different rRNA gene primers for bacteria, archaea, and eukaryotes, precluding comparisons across size fractions or domains. On average, bacteria contributed 71%, eukaryotes 19%, and archaea 8% to rRNA gene abundance, though eukaryotes contributed 32% at latitudes > 40. GRUMP is publicly available on the Simons Collaborative Marine Atlas Project (CMAP), promoting the global comparison of marine microbial dynamics.
ABSTRACT A thorough understanding of ecosystem functioning in the Arctic Ocean, a region under severe threat by climate change, requires detailed studies on linkages between biodiversity and ecosystem stability. The identification of keystone species with special relevance for ecosystem stability is of great importance, yet difficult to achieve with established community assessments. In the case of microbes, metabarcoding and metagenomics offer fundamental insights into community structure and function, yet remain limited regarding the ecological relevance of individual taxa. To overcome this limitation, we have developed an analytical approach based on three different methods: Co-Occurrence Networks, Convergent Cross Mapping, and Energy Landscape Analysis. These methods enable the identification of seasonal communities in microbial ecosystems, elucidate their interactions, and predict potential stable community configurations under varying environmental conditions. Combining the outcomes of these three methods allowed us to define 38 keystone species in the Arctic Fram Strait that represent different trophic modes within the food web, and might signify indicator for ecosystem functionality under the impact of environmental change. Our research reveals a clear seasonal pattern in phytoplankton composition, with distinct assemblages characterizing the phases of carbon fixation (polar day) and consumption (polar night). Species interactions exhibited strong seasonality, with significant influence of summer communities on winter communities but not vice versa. Spring harbored two distinct groups: consumers (heterotrophs), strongly linked to polar night, and photoautotrophs (mainly Bacillariophyta). These groups are not causally related, suggesting a “winter reset” with selective effects that facilitates a new blooming period, allowing survivors of the dark phase to emerge. Energy Landscape Analysis showed that winter communities are more stable than summer communities. In summary, the ecological landscape of the Fram Strait can be categorized into two distinct phases: a production phase governed by specialized organisms that are highly responsive to environmental variability, and a heterotrophic phase dominated by generalist species with enhanced resilience.
Abstract Submesoscale eddies and fronts are recognized as important components of oceanic mixing and energy fluxes. These submesoscale phenomena occur in the surface ocean for a period of a few days on scales between several hundred meters and a few tens of kilometers. Remote sensing and modeling suggest that they may influence marine ecosystem dynamics, but their limited temporal and spatial scales make them challenging for observation and in situ sampling. Here, the study of a submesoscale filament in summerly Arctic waters (depth 0 - 400 m) revealed enhanced vertical mixing of Polar and Atlantic water masses, resulting in a ca. 4 km wide and ca. 50 km long filament with distinct physical and biogeochemical conditions. Compared to the surrounding waters the filament was characterized by a distinct phytoplankton bloom dominated by diatoms and two-fold higher bacterioplankton cell densities. High-throughput 16S rRNA gene sequencing of both bacterioplankton communities revealed 3-4 orders of magnitude higher sequence abundance of Synechococcus inside the filament, as well as tenfold higher sequence abundance of taxonomic groups typically found during summertime in aging phytoplankton blooms (e.g., Flavobacteriales ). In contrast, the surrounding waters contained severalfold higher sequence abundance of winterly taxonomic groups that are also associated with polar water masses (e.g., SAR202 clade). Altogether, our results show that physical submesoscale processes in the ocean can shape distinct biogeochemical conditions and microbial communities within a few kilometers. Furthermore, our results underline the importance of such submesoscale features for our understanding of surface ocean diversity and biogeochemical processes.
Prokaryotic CRISPR-Cas systems confer resistance to viral infection and thus mediate bacteria-phage interactions. However, the distribution and functional diversity of CRISPRs among environmental bacteria remains largely unknown. Here, comparative genomics of 75 Salinispora strains provided insight into the diversity and distribution of CRISPR-Cas systems in a cosmopolitan marine actinomycete genus. CRISPRs were found in all Salinispora strains, with the majority containing multiple loci and different Cas array subtypes. Of the six subtypes identified, three have not been previously described. A lower prophage frequency in S. arenicola was associated with a higher fraction of spacers matching Salinispora prophages compared to S. tropica, suggesting differing defensive capacities between Salinispora species. The occurrence of related prophages in strains from distant locations, as well as spacers matching those prophages inserted throughout spacer arrays, indicate recurring encounters with widely distributed phages over time. Linkages of CRISPR features with Salinispora microdiversity pointed to subclade-specific contacts with mobile genetic elements (MGEs). This included lineage-specific spacer deletions or insertions, which may reflect weak selective pressures to maintain immunity or distinct temporal interactions with MGEs, respectively. Biogeographic patterns in spacer and prophage distributions support the concept that Salinispora spp. encounter localized MGEs. Moreover, the presence of spacers matching housekeeping genes suggests that CRISPRs may have functions outside of viral defense. This study provides a comprehensive examination of CRISPR-Cas systems in a broadly distributed group of environmental bacteria. The ubiquity and diversity of CRISPRs in Salinispora suggests that CRISPR-mediated interactions with MGEs represent a major force in the ecology and evolution of this cosmopolitan marine actinomycete genus.
Visible surface films, termed slicks, can extensively cover freshwater and marine ecosystems, with coastal regions being particularly susceptible to their presence. The sea-surface microlayer (SML), the upper 1-mm at the air-water interface in slicks (herein slick SML) harbors a distinctive bacterial community, but generally little is known about SML viruses. Using flow cytometry, metagenomics, and cultivation, we characterized viruses and bacteria in a brackish slick SML in comparison to non-slick SML as well as seawater below slick and non-slick areas (subsurface water = SSW). Size-fractionated filtration of all samples distinguished viral attachment to hosts and particles. The slick SML contained higher abundances of virus-like particles, prokaryotic cells, and dissolved organic carbon compared to non-slick SML and SSW. The community of 428 viral operational taxonomic units (vOTUs), 426 predicted as lytic, distinctly differed across all size fractions in the slick SML compared to non-slick SML and SSW. Specific metabolic profiles of bacterial metagenome-assembled genomes and isolates in the slick SML included a prevalence of genes encoding motility and carbohydrate-active enzymes (CAZymes). Several vOTUs were enriched in slick SML, and many virus variants were associated with particles. Nine vOTUs were only found in slick SML, six of them being targeted by slick SML-specific clustered-regularly interspaced short palindromic repeats (CRISPR) spacers likely originating from Gammaproteobacteria. Moreover, isolation of three previously unknown lytic phages for Alishewanella sp. and Pseudoalteromonas tunicata, abundant and actively replicating slick SML bacteria, suggests that viral activity in slicks contributes to biogeochemical cycling in coastal ecosystems.
Polysaccharides are major components of macroalgal and phytoplankton biomass and constitute a large fraction of the organic matter produced and degraded in the ocean. Until recently, however, our knowledge of marine polysaccharides was limited due to their great structural complexity, the correspondingly complicated enzymatic machinery used by microbial communities to degrade them, and a lack of readily applied means to isolate andcharacterize polysaccharides in detail. Advances in carbohydrate chemistry, bioinformatics, molecular ecology, and microbiology have led to new insights into the structures of polysaccharides, the means by which they are degraded by bacteria, and the ecology of polysaccharide production and decomposition. Here, we survey current knowledge, discuss recent advances, and present a new conceptual model linking polysaccharide structural complexity and abundance to microbially driven mechanisms of polysaccharide processing. We conclude by highlighting specific future research foci that will shed light on this central but poorly characterized component of the marine carbon cycle.
The ocean moderates the world's climate through absorption of heat and carbon, but how much carbon the ocean will continue to absorb remains unknown. The North Atlantic Ocean west (Baffin Bay/Labrador Sea) and east (Fram Strait/Greenland Sea) of Greenland features the most intense absorption of anthropogenic carbon globally; the biological carbon pump (BCP) contributes substantially. As Arctic sea-ice melts, the BCP changes, impacting global climate and other critical ocean attributes (e.g. biodiversity). Full understanding requires year-round observations across a range of ice conditions. Here we present such observations: autonomously collected Eulerian continuous 24-month time-series in Fram Strait. We show that, compared to ice-unaffected conditions, sea-ice derived meltwater stratification slows the BCP by 4 months, a shift from an export to a retention system, with measurable impacts on benthic communities. This has implications for ecosystem dynamics in the future warmer Arctic where the seasonal ice zone is expected to expand.
