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Proteorhodopsins (PR) are light-driven proton pumps widely distributed in bacterioplankton. Although they have been thoroughly studied for more than a decade, it is still unclear how the proton motive force (pmf) generated by PR is used in most organisms. Notably, very few PR-containing bacteria show growth enhancement in the light. It has been suggested that the presence of specific functions within a genome may define the different PR-driven light responses. Thus, comparing closely related organisms that respond differently to light is an ideal setup to identify the mechanisms involved in PR light-enhanced growth. Here, we analyzed the transcriptomes of three PR-harboring Flavobacteria strains of the genus Dokdonia: Dokdonia donghaensis DSW-1 super(T), Dokdonia MED134 and Dokdonia PRO95, grown in identical seawater medium in light and darkness. Although only DSW-1 super(T) and MED134 showed light-enhanced growth, all strains expressed their PR genes at least 10 times more in the light compared with dark. According to their genomes, DSW-1 super(T) and MED134 are vitamin-B sub(1) auxotrophs, and their vitamin-B sub(1) TonB-dependent transporters (TBDT), accounted for 10-18% of all pmf-dependent transcripts. In contrast, the expression of vitamin-B sub(1) TBDT was 10 times lower in the prototroph PRO95, whereas its vitamin-B sub(1) synthesis genes were among the highest expressed. Our data suggest that light-enhanced growth in DSW-1 super(T) and MED134 derives from the use of PR-generated pmf to power the uptake of vitamin-B sub(1), essential for central carbon metabolism, including the TCA cycle. Other pmf-generating mechanisms available in darkness are probably insufficient to power transport of enough vitamin-B sub(1) to support maximum growth of these organisms.

The regeneration of bioavailable phosphate from immobilized organophosphorus represents a key process in the global phosphorus cycle and is facilitated by enzymes known as phosphatases. Most bacteria possess at least one of three phosphatases with broad substrate specificity, known as PhoA, PhoX, and PhoD, whose activity is optimal under alkaline conditions. The production and activity of these phosphatases is repressed by phosphate availability. Therefore, they are only fully functional when bacteria experience phosphorus-limiting growth conditions. Here, we reveal a previously overlooked phosphate-insensitive phosphatase, PafA, prevalent in Bacteroidetes, which is highly abundant in nature and represents a major route for the regeneration of environmental phosphate. Using the enzyme from Flavobacterium johnsoniae, we show that PafA is highly active toward phosphomonoesters, is fully functional in the presence of excess phosphate, and is essential for growth on phosphorylated carbohydrates as a sole carbon source. These distinct properties of PafA may expand the metabolic niche of Bacteroidetes by enabling the utilization of abundant organophosphorus substrates as C and P sources, providing a competitive advantage when inhabiting zones of high microbial activity and nutrient demand. PafA, which is constitutively synthesized by soil and marine flavobacteria, rapidly remineralizes phosphomonoesters releasing bioavailable phosphate that can be acquired by neighboring cells. The pafA gene is highly diverse in plant rhizospheres and is abundant in the global ocean, where it is expressed independently of phosphate availability. PafA therefore represents an important enzyme in the context of global biogeochemical cycling and has potential applications in sustainable agriculture.

Key Points Phytoplankton are the most abundant primary producers in the oceans, and phytoplankton blooms are recognizable signs of the annual productivity cycle in aquatic systems. Phytoplankton blooms contain dense and diverse heterotrophic bacterial populations that determine the fate of much of the carbon that is fixed by these primary producers. This is achieved by the transformation of phytoplankton-derived organic matter, which returns carbon to the atmosphere as CO 2 and converts carbon to bacterial biomass, which enters the marine food web or renders it resistant to microbial degradation, such that it contributes to a vast pool of recalcitrant carbon in the ocean. Although blooms vary in terms of phytoplankton composition and environmental conditions, a limited number of bacterial taxa dominate bloom-associated microbial communities. The most frequently observed bacteria belong to the Flavobacteriia and Proteobacteria. Cultivated representatives of both flavobacteria and roseobacters are currently the main models that are used to study phytoplankton–bacteria interactions. These two lineages show substantial metabolic versatility, which seems to fuel these interactions. Culture-based studies of roseobacters suggest that they form more intimate associations with specific phytoplankton than flavobacteria. Specific physiological processes that have been identified in cultured representatives and are supported by metagenomic data from natural populations have been proposed to facilitate these interactions. These include the production of secondary metabolites, catabolism of various phytoplankton-derived low molecular weight compounds and cell surface structures that facilitate cellular adhesion. Genomic, metatranscriptomic and metaproteomic data suggest that flavobacteria are particularly well equipped to use the high molecular weight components of phytoplankton-derived material. Other flavobacterial physiologies, including cell adhesion and motility, may be important in facilitating interactions between flavobacteria and phytoplankton. Marine phytoplankton blooms are annual spring events that are accompanied by a surge in heterotrophic bacteria, primarily roseobacters, flavobacteria and members of the Gammaproteobacteria, which recycle most of the carbon that is fixed by the primary producers. In this Review, Buchan et al . describe the emerging physiological features and functions of these bacterial communities and their interactions with phytoplankton. Marine phytoplankton blooms are annual spring events that sustain active and diverse bloom-associated bacterial populations. Blooms vary considerably in terms of eukaryotic species composition and environmental conditions, but a limited number of heterotrophic bacterial lineages — primarily members of the Flavobacteriia, Alphaproteobacteria and Gammaproteobacteria — dominate these communities. In this Review, we discuss the central role that these bacteria have in transforming phytoplankton-derived organic matter and thus in biogeochemical nutrient cycling. On the basis of selected field and laboratory-based studies of flavobacteria and roseobacters, distinct metabolic strategies are emerging for these archetypal phytoplankton-associated taxa, which provide insights into the underlying mechanisms that dictate their behaviours during blooms.

We employed high frequency sampling to determine the major factors modulating microbial food-web composition and dynamics through the spring phytoplankton bloom and clear-water phases in a freshwater reservoir. We examined effects of a changing trophic structure of the planktonic community cascading fromthe level of zooplankton, through phytoplankton composition and exudation rates to the level of growth responses and losses to grazers of phylogenetically narrow bacterial lineages. Specific probes for fluorescence in situ hybridization (FISH) revealed important short-lived peaks of genus-like (Fluviiciola sp. and Limnohabitans spp.) or even taxonomically narrower populations of Betaproteobacteria and Flavobacteria (such as FlavB and Flav2 lineages). Protozoan grazing on bacterioplankton was studied by using fluorescently labeled bacteria and by direct analyses of FISH-probe–targeted bacterial phylotypes in flagellate food vacuoles. Evaluations of selective bacterivory, growth responses, and cell biovolumes of various bacterial groups during the spring bloom indicated that certain bacterial groups such as Limnohabitans can contribute to carbon flow to the grazer food chain up to 10-fold more than similarly abundant small cells from the Ac1 lineage of Actinobacteria. During the clear-water phase, filter-feeding cladocera had dominant effects on bacterioplankton abundance and community dynamics, likely through direct grazing on larger bacteria along with altering major substrate pools (via e.g., the herbivores’ sloppy feeding on algae). Fine-temporal resolution data revealed several environmental scenarios, in which the interplay of distinct top-down and bottom-up factors resulted in a competitive advantage of particular bacterial lineages.

Phytoplankton blooms characterize temperate ocean margin zones in spring. We investigated the bacterioplankton response to a diatom bloom in the North Sea and observed a dynamic succession of populations at genus-level resolution. Taxonomically distinct expressions of carbohydrate-active enzymes (transporters; in particular, TonB-dependent transporters) and phosphate acquisition strategies were found, indicating that distinct populations of Bacteroidetes, Gammaproteobacteria, and Alphaproteobacteria are specialized for successive decomposition of algal-derived organic matter. Our results suggest that algal substrate availability provided a series of ecological niches in which specialized populations could bloom. This reveals how planktonic species, despite their seemingly homogeneous habitat, can evade extinction by direct competition.

Dissolved organic nitrogen (DON) supports a significant amount of heterotrophic production in the ocean. Yet, to date, the identity and diversity of microbial groups that transform DON are not well understood. To better understand the organisms responsible for transforming high molecular weight (HMW)-DON in the upper ocean, isotopically labeled protein extract from Micromonas pusilla , a eukaryotic member of the resident phytoplankton community, was added as substrate to euphotic zone water from the central California Current system. Carbon and nitrogen remineralization rates from the added proteins ranged from 0.002 to 0.35 μmol C l −1 per day and 0.03 to 0.27 nmol N l −1 per day. DNA stable-isotope probing (DNA-SIP) coupled with high-throughput sequencing of 16S rRNA genes linked the activity of 77 uncultivated free-living and particle-associated bacterial and archaeal taxa to the utilization of Micromonas protein extract. The high-throughput DNA-SIP method was sensitive in detecting isotopic assimilation by individual operational taxonomic units (OTUs), as substrate assimilation was observed after only 24 h. Many uncultivated free-living microbial taxa are newly implicated in the cycling of dissolved proteins affiliated with the Verrucomicrobia, Planctomycetes, Actinobacteria and Marine Group II (MGII) Euryarchaeota. In addition, a particle-associated community actively cycling DON was discovered, dominated by uncultivated organisms affiliated with MGII, Flavobacteria, Planctomycetes, Verrucomicrobia and Bdellovibrionaceae. The number of taxa assimilating protein correlated with genomic representation of TonB-dependent receptor (TBDR)-encoding genes, suggesting a possible role of TBDR in utilization of dissolved proteins by marine microbes. Our results significantly expand the known microbial diversity mediating the cycling of dissolved proteins in the ocean.

Microbial activities that affect global oceanographic and atmospheric processes happen throughout the water column, yet the long-term ecological dynamics of microbes have been studied largely in the euphotic zone and adjacent seasonally mixed depths. We investigated temporal patterns in the community structure of free-living bacteria, by sampling approximately monthly from 5 m, the deep chlorophyll maximum (∼15–40 m), 150, 500 and 890 m, in San Pedro Channel (maximum depth 900 m, hypoxic below ∼500 m), off the coast of Southern California. Community structure and biodiversity (inverse Simpson index) showed seasonal patterns near the surface and bottom of the water column, but not at intermediate depths. Inverse Simpson’s index was highest in the winter in surface waters and in the spring at 890 m, and varied interannually at all depths. Biodiversity appeared to be driven partially by exchange of microbes between depths and was highest when communities were changing slowly over time. Meanwhile, communities from the surface through 500 m varied interannually. After accounting for seasonality, several environmental parameters co-varied with community structure at the surface and 890 m, but not at the intermediate depths. Abundant and seasonally variable groups included, at 890 m, Nitrospina , Flavobacteria and Marine Group A. Seasonality at 890 m is likely driven by variability in sinking particles, which originate in surface waters, pass transiently through the middle water column and accumulate on the seafloor where they alter the chemical environment. Seasonal subeuphotic groups are likely those whose ecology is strongly influenced by these particles. This surface-to-bottom, decade-long, study identifies seasonality and interannual variability not only of overall community structure, but also of numerous taxonomic groups and near-species level operational taxonomic units.

Aims The present study was planned to investigate the diversity of 1-aminocyclopropane-1-carboxylate (ACC) deaminase producing bacteria from the rhizosphere of wheat plants and subsequent evaluation of selected PGPR on growth enhancement of wheat seedlings under drought and saline conditions. Methods ACC deaminase producing plant growth promoting rhizobacteria (PGPR) were isolated from the rhizosphere of wheat and identified using 16S rRNA gene sequence analysis. Isolates were evaluated for various direct and indirect plant growth promoting (PGP) traits. Plant inoculation experiment was conducted using isolates IG 19 and IG 22 in wheat to assess their plant growth promotion potential under salinity and drought stress. Results Thirty-eight ACC deaminase producing PGPR were isolated which belonged to 12 distinct genera and falling into four phyla γ-proteobacteria, β-proteobacteria, Flavobacteria and Firmicutes. Klebsiella sp. was the most abundant genera and followed by Enterobacter sp. The isolates exhibited ACC deaminase activities ranging from 0.106-0.980 μM α-ketobutyrate μg protein⁻¹ h⁻¹. The isolates showed multiple PGP traits such as IAA production, phosphate, zinc, potassium solubilization and siderophore production. Enterobacter cloacae (IG 19) and Citrobacter sp. (IG 22) inoculated wheat seedlings showed notable increases in fresh and dry biomass under non-stress as well as under stressed condition. Conclusion To the best of our knowledge this is the first report of presence of ACC deaminase activity and other PGP traits from the genus Citrobacter and Empedobacter. Our finding revealed that the γ-proteobacteria group dominated the wheat rhizosphere. Plant inoculation with PGPR could be a sustainable approach to alleviate abiotic stresses in wheat plants. These native PGPR isolates could be used as potential biofertilizers for sustainable agriculture.

Light-activated, ion-pumping rhodopsins are broadly distributed among many different bacteria and archaea inhabiting the photic zone of aquatic environments. Bacterial proton- or sodium-translocating rhodopsins can convert light energy into a chemiosmotic force that can be converted into cellular biochemical energy, and thus represent a widespread alternative form of photoheterotrophy. Here we report that the genome of the marine flavobacterium Nonlabens marinus S1-08 ᵀ encodes three different types of rhodopsins: Nonlabens marinus rhodopsin 1 (NM-R1), Nonlabens marinus rhodopsin 2 (NM-R2), and Nonlabens marinus rhodopsin 3 (NM-R3). Our functional analysis demonstrated that NM-R1 and NM-R2 are light-driven outward-translocating H ⁺ and Na ⁺ pumps, respectively. Functional analyses further revealed that the light-activated NM-R3 rhodopsin pumps Cl ⁻ ions into the cell, representing the first chloride-pumping rhodopsin uncovered in a marine bacterium. Phylogenetic analysis revealed that NM-R3 belongs to a distinct phylogenetic lineage quite distant from archaeal inward Cl ⁻-pumping rhodopsins like halorhodopsin, suggesting that different types of chloride-pumping rhodopsins have evolved independently within marine bacterial lineages. Taken together, our data suggest that similar to haloarchaea, a considerable variety of rhodopsin types with different ion specificities have evolved in marine bacteria, with individual marine strains containing as many as three functionally different rhodopsins.