Production of extracellular vesicles with light‐induced proton pump activity by proteorhodopsin‐containing marine bacteria

Kwon, Yong Hyun; Patra, Ajit Kumar; Chiura, Hiroshi Xavier; Kim, Sang-Jin

doi:10.1002/mbo3.808

Cited by 10 publications

(7 citation statements)

References 41 publications

(65 reference statements)

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“…In addition, some microbial cells were covered with pellets, which could be membrane vesicle-like structures ( Figure 1B ). Membrane vesicles are common for many bacteria and have widely diverse functions, such as specialized “organ-like” parts, which may have, e.g., proton-pump activity, and can be used for distribution of hydrophobic signaling molecules, mineralization of toxins, accumulation of various elements when colonizing rock surfaces, and cell surface shedding linked to the reduction of metals and weathering, e.g., black shale ( Matlakowska and Sklodowska, 2011 ; Manning and Kuehn, 2013 ; Shao et al, 2014 ; Toyofuku et al, 2015 ; Keren et al, 2017 ; Brameyer et al, 2018 ; Kwon et al, 2019 ).…”

Section: Discussionmentioning

confidence: 99%

Epilithic Microbial Community Functionality in Deep Oligotrophic Continental Bedrock

Nuppunen-Puputti

Kietäväinen

Raulio³

et al. 2022

Front. Microbiol.

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The deep terrestrial biosphere hosts vast sessile rock surface communities and biofilms, but thus far, mostly planktic communities have been studied. We enriched deep subsurface microbial communities on mica schist in microcosms containing bedrock groundwater from the depth of 500 m from Outokumpu, Finland. The biofilms were visualized using scanning electron microscopy, revealing numerous different microbial cell morphologies and attachment strategies on the mica schist surface, e.g., bacteria with outer membrane vesicle-like structures, hair-like extracellular extensions, and long tubular cell structures expanding over hundreds of micrometers over mica schist surfaces. Bacterial communities were analyzed with amplicon sequencing showing that Pseudomonas, Desulfosporosinus, Hydrogenophaga, and Brevundimonas genera dominated communities after 8–40 months of incubation. A total of 21 metagenome assembled genomes from sessile rock surface metagenomes identified genes involved in biofilm formation, as well as a wide variety of metabolic traits indicating a high degree of environmental adaptivity to oligotrophic environment and potential for shifting between multiple energy or carbon sources. In addition, we detected ubiquitous organic carbon oxidation and capacity for arsenate and selenate reduction within our rocky MAGs. Our results agree with the previously suggested interaction between the deep subsurface microbial communities and the rock surfaces, and that this interaction could be crucial for sustaining life in the harsh anoxic and oligotrophic deep subsurface of crystalline bedrock environment.

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Section: Discussionmentioning

confidence: 99%

Epilithic Microbial Community Functionality in Deep Oligotrophic Continental Bedrock

Nuppunen-Puputti

Kietäväinen

Raulio³

et al. 2022

Front. Microbiol.

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“…Marine viruses have previously been shown to migrate to CsCl densities between 1.45 and 1.55 g mL −1 (Lawrence and Steward 2010), while DNA has been reported around 1.63-1.76 g mL −1 (Wells and Larson 1972;Lueders et al 2004). Marine microbial vesicles have been reported from 1.19 to 1.35 g mL −1 in CsCl (Choi et al 2015;Kwon et al 2019), congruent with previous reports of membrane-enclosed DNA migrating around 1.30 g mL −1 (Anderson et al 1966). The density of each fraction was determined gravimetrically and the volume measured using a positive displacement pipet.…”

Section: Density Gradient Separationmentioning

confidence: 99%

A method for characterizing dissolved DNA and its application to the North Pacific Subtropical Gyre

Linney

Schvarcz

Steward

et al. 2021

Limnology & Ocean Methods

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Dissolved DNA (D-DNA) is a ubiquitous component of dissolved organic matter in aquatic systems. It is operationally defined as the DNA that passes a membrane filter and thus includes pools of truly dissolved "free" DNA (F-DNA), virion encapsidated DNA, DNA within membrane vesicles, and possibly other bound forms, each with different sources and lability. We investigated whether filtration (< 0.1 μm), concentration by tangential flow ultrafiltration (> 30 kDa), and fractionation in an equilibrium buoyant density gradient could be used to discriminate the mass contributions of the different pools of filterable DNA in seawater. Spike-in experiments with a known range of DNA standards (75-20,000 bp) indicated that this method results in high recoveries of F-DNA (68-86%) with minimal degradation. Application of the fractionation method to seawater samples collected from the oligotrophic North Pacific Ocean followed by analysis of fractions (epifluorescence and electron microscopy, DNase digestion) suggested that the low-density fractions (1.30-1.35 g mL −1) were dominated by vesicle-like particles, mid-density fractions (1.45-1.55 g mL −1) by virus-like particles, and high-density fractions (1.60-1.70 g mL −1) by F-DNA. The estimated concentration of DNA that is either F-DNA, in viruses, or in vesicles was 0.13, 0.14, and 0.08 μg L −1 , respectively in the euphotic zone and 0.09, 0.04, and 0.03 μg L −1 , respectively in the mesopelagic zone. The approach described should be useful for more detailed investigations of the abundance, dynamics, and sources of DNA in the distinct pools that comprise filterable DNA in aquatic environments. Dissolved DNA (D-DNA)-a highly labile and nutrient-rich component of dissolved organic material (DOM)-is ubiquitous in all aquatic habitats investigated to date, including freshwater rivers and lakes (Pillai and Ganguly 1972), coastal marine and estuarine systems (DeFlaun et al. 1986), sediments (Dell'Anno et al. 2002), and the open ocean (Karl and Bailiff 1989; Brum 2005). Concentrations of D-DNA often represent a substantial fraction of the total DNA (DeFlaun et al. 1987; Karl and Bailiff 1989), especially in the open ocean. Spatial patterns of D-DNA concentrations in the ocean are similar to those of total microbial biomass and total DOM, decreasing with distance from shore and with depth (DeFlaun et al. 1987; Karl and Bailiff 1989; Weinbauer et al. 1993, 1995). The concentration and bioavailability of D-DNA has both evolutionary and ecological significance. Double stranded D-DNA has the potential to alter the genetic make-up of microbial cells by the process of natural transformation (Hermansson and Linberg 1994) or, if hydrolyzed, can serve as a source of nitrogen and phosphorus (Jørgensen and Jacobsen 1996), macronutrients that are often limiting to microorganisms in open ocean ecosystems (Karl and Church 2014). As a consequence, there has been considerable interest in developing methods to investigate the nature and dynamics of this component of the larger DOM pool. Methods to stud...

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“…Previous estimates of MV production in pelagic marine bacteria range from few to several dozen MVs per bacterial cell (Biller et al 2014 , Kwon et al 2019 , 2022 ). Based on temporal changes in cell and MV abundances, the six strains of A. macleodii showed overall net MV production rates within the same order of magnitude to previous observations (Fig.…”

Section: Resultsmentioning

confidence: 99%

Characterization of membrane vesicles in Alteromonas macleodii indicates potential roles in their copiotrophic lifestyle

et al. 2022

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Bacterial membrane vesicles (MVs) are abundant in the oceans, but their potential functional roles remain unclear. In this study we characterized MV production and protein content of six strains of Alteromonas macleodii, a cosmopolitan marine bacterium. A. macleodii strains varied in their MV production rates, with some releasing up to 30 MVs per cell per generation. Microscopy imaging revealed heterogenous MV morphologies, including some MVs aggregated within larger membrane structures. Proteomic characterization revealed that A. macleodii MVs are rich in membrane proteins related to iron and phosphate uptake, as well as proteins with potential functions in biofilm formation. Furthermore, MVs harbored ectoenzymes, such as aminopeptidases and alkaline phosphatases, which comprised up to 20% of the total extracellular enzymatic activity. Our results suggest that A. macleodii MVs may support its growth through generation of extracellular “hotspots” that facilitate access to essential substrates. This study provides an important basis to decipher the ecological relevance of MVs in heterotrophic marine bacteria.

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Production of extracellular vesicles with light‐induced proton pump activity by proteorhodopsin‐containing marine bacteria

Cited by 10 publications

References 41 publications

Epilithic Microbial Community Functionality in Deep Oligotrophic Continental Bedrock

Epilithic Microbial Community Functionality in Deep Oligotrophic Continental Bedrock

A method for characterizing dissolved DNA and its application to the North Pacific Subtropical Gyre

Characterization of membrane vesicles in Alteromonas macleodii indicates potential roles in their copiotrophic lifestyle

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