Niches of two polysaccharide-degrading <i>Polaribacter</i> isolates from the North Sea during a spring diatom bloom

Xing, Peng; Hahnke, Richard L.; Unfried, Frank; Markert, Stephanie; Huang, Sixing; Barbeyron, Tristan; Harder, Jens; Becher, Dörte; Schweder, Thomas; Glöckner, Frank Oliver; Amann, Rudolf; Teeling, Hanno

doi:10.1038/ismej.2014.225

Cited by 169 publications

(202 citation statements)

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“…Peptides were eluted from the gel pieces in a sonication bath and purified using ZipTips (Millipore) according to the manufacturer's recommendations. As described previously 60 , peptide mixes were subjected to separation using reversed-phase C18 column chromatography on a nanoACQUITY-UPLC system (Waters). Mass spectrometry (MS)-and tandem mass spectrometry (MS/MS) data were acquired using an online-coupled LTQOrbitrap mass spectrometer (Thermo Fisher Scientific).…”

Section: Methodsmentioning

confidence: 99%

Nitrogen fixation in a chemoautotrophic lucinid symbiosis

et al. 2016

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The shallow water bivalve Codakia orbicularis lives in symbiotic association with a sulfur-oxidizing bacterium in its gills. The endosymbiont fixes CO 2 and thus generates organic carbon compounds, which support the host's growth. To investigate the uncultured symbiont's metabolism and symbiont-host interactions in detail we conducted a proteogenomic analysis of purified bacteria. Unexpectedly, our results reveal a hitherto completely unrecognized feature of the C. orbicularis symbiont's physiology: the symbiont's genome encodes all proteins necessary for biological nitrogen fixation (diazotrophy). Expression of the respective genes under standard ambient conditions was confirmed by proteomics. Nitrogenase activity in the symbiont was also verified by enzyme activity assays. Phylogenetic analysis of the bacterial nitrogenase reductase NifH revealed the symbiont's close relationship to free-living nitrogen-fixing Proteobacteria from the seagrass sediment. The C. orbicularis symbiont, here tentatively named 'Candidatus Thiodiazotropha endolucinida', may thus not only sustain the bivalve's carbon demands. C. orbicularis may also benefit from a steady supply of fixed nitrogen from its symbiont-a scenario that is unprecedented in comparable chemoautotrophic symbioses. Mutualistic associations between marine invertebrates and sulfur-oxidizing (thiotrophic) bacteria are a well-documented and widespread phenomenon in a variety of sulfidic habitats ranging from hydrothermal vents to shallow-water coastal ecosystems 1-3 . Thioautotrophic symbionts generate energy through sulfide oxidation and provide their hosts with organic carbon. In the Lucinidae, a diverse family of marine bivalves, all members are obligatorily dependent on their bacterial gill endosymbionts after larval development and metamorphosis 4 . The shallowwater lucinid Codakia orbicularis, which lives in the sediment beneath the tropical seagrass Thalassia testudinum along the Caribbean and Western Atlantic coast 5 , harbours a single species of endosymbionts in its gills 6 . The symbiont has been shown to be newly acquired by each clam generation 7,8 from a pool of freeliving symbiosis-competent bacteria in the environment 9 , rather than being inherited from clam parents. C. orbicularis appears not to release its endosymbionts, even under adverse conditions, but can digest them as a source of nutrition [10][11][12] . Moreover, bacterial cell division seems to be inhibited inside the host tissue. The majority of the symbiont population was shown to be polyploid (that is, containing multiple genome copies), while dividing symbiont cell stages are very rarely observed in host bacteriocytes 13 . The host undoubtedly benefits from the symbiont both by way of detoxification of its sulfidic environment and by supply of organic compounds through the bacterial Calvin-Benson cycle. It remains questionable, however, whether the symbiont gains any advantage from this association in evolutionary terms 11 .Biological nitrogen fixation (diazotrophy) is the conversion of ...

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Section: Methodsmentioning

confidence: 99%

Nitrogen fixation in a chemoautotrophic lucinid symbiosis

et al. 2016

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“…The bacterium was tested for the Gram reaction by using the Gram-staining method (45). Cell morphology was examined by optical microscopy (BX40 microscope; Olympus) and transmission electron microscopy (JEM-1230 microscope; JEOL) using exponentially growing cells that were incubated on MA for 24 h. Growth at various NaCl concentrations (0.5, 1, 1.5, 2, 2.5, 3, 3.5, 4, 6, 8, 10, and 12% [wt/vol]), a range of pHs (pH 5.0 to 10.5, with an interval of 0.5), and a range of temperatures (4,10,15,20,25,28,30,35,37,40,42, and 45°C) was carried out according to a protocol described previously (46). Catalase and oxidase were detected as described previously (45).…”

Section: Methodsmentioning

confidence: 99%

“…Hel1_33_49 and Hel1_85 (35), have the structure and function of polysaccharide utilization loci (PUL) been reported. The first report of PUL in marine Bacteroidetes was for Zobellia galactanivorans, which contains two PUL with alginate lyases that are induced by alginate (30).…”

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confidence: 99%

Isolation and Complete Genome Sequence of Algibacter alginolytica sp. nov., a Novel Seaweed-Degrading Bacteroidetes Bacterium with Diverse Putative Polysaccharide Utilization Loci

Sun

Zhang

et al. 2016

Appl Environ Microbiol

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eThe members of the phylum Bacteroidetes are recognized as some of the most important specialists for the degradation of polysaccharides. However, in contrast to research on Bacteroidetes in the human gut, research on polysaccharide degradation by marine Bacteroidetes is still rare. The genus Algibacter belongs to the Flavobacteriaceae family of the Bacteroidetes, and most species in this genus are isolated from or near the habitat of algae, indicating a preference for the complex polysaccharides of algae. In this work, a novel brown-seaweed-degrading strain designated HZ22 was isolated from the surface of a brown seaweed (Laminaria japonica). On the basis of its physiological, chemotaxonomic, and genotypic characteristics, it is proposed that strain HZ22 represents a novel species in the genus Algibacter with the proposed name Algibacter alginolytica sp. nov. The genome of strain HZ22, the type strain of this species, harbors 3,371 coding sequences (CDSs) and 255 carbohydrate-active enzymes (CAZymes), including 104 glycoside hydrolases (GHs) and 18 polysaccharide lyases (PLs); this appears to be the highest proportion of CAZymes (ϳ7.5%) among the reported strains in the class Flavobacteria. Seventeen polysaccharide utilization loci (PUL) are predicted to be specific for marine polysaccharides, especially algal polysaccharides from red, green, and brown seaweeds. In particular, PUL N is predicted to be specific for alginate. Taking these findings together with the results of assays of crude alginate lyases, we prove that strain HZ22 T can completely degrade alginate. This work reveals that strain HZ22 T has good potential for the degradation of algal polysaccharides and that the structure and related mechanism of PUL in strain HZ22T are worth further research. Members of the phylum Bacteroidetes, formerly also known as the Cytophaga-Flavobacteria-Bacteroides cluster, constitute one of the major groups of marine heterotrophic bacterioplankton (1, 2). They have been found in various marine habitats, including coastal sediments (3), coastal waters (4, 5), hydrothermal vents (6, 7), and open ocean waters (8-10). In previous studies, marine Bacteroidetes have been reported as important contributors to the utilization of biopolymers such as polysaccharides and proteins (2,(11)(12)(13)(14). As a result, marine Bacteroidetes are assumed to play an important role in the degradation of algae. Marine phytoplankton have been estimated to be responsible for about 50% of global net primary production (15). Polysaccharides constitute a substantial fraction of the primary production from marine phytoplankton. Algae can be an important source of polysaccharides. Brown seaweeds, a traditional and plentiful mariculture product in East Asia, make up a large proportion of the total biomass of algae and synthesize a wide variety of compounds, such as alginate, fucoidan, laminarin, and mannitol (16). Among these compounds, alginate has been assumed to be a potential source for bioethanol production (17-19).The genus Algibacter belongs...

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“…All of these polysaccharides are found in marine environments, and/or enzymes and genes corresponding to their hydrolysis have been identified in marine prokaryotes (e.g., Alderkamp et al, 2007;Wegner et al, 2013;Xing et al, 2015). Furthermore, the activities of enzymes hydrolyzing these substrates have been detected in a wide variety of marine environments (e.g., Arnosti, 2008;Arnosti et al, 2009Arnosti et al, , 2011.…”

Section: Polysaccharide Hydrolysis Measurementsmentioning

confidence: 99%

Heterotrophic Extracellular Enzymatic Activities in the Atlantic Ocean Follow Patterns Across Spatial and Depth Regimes

Hoarfrost

Arnosti

2017

Front. Mar. Sci.

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Heterotrophic microbial communities use extracellular enzymes to initialize degradation of high molecular weight organic matter in the ocean. The potential of microbial communities to access organic matter, and the resultant rates of hydrolysis, affect the efficiency of the biological pump as well as the rate and location of organic carbon cycling in surface and deep waters. In order to investigate spatial-and depth-related patterns in microbial enzymatic capacities in the ocean, we measured hydrolysis rates of six high-molecular-weight polysaccharides and two low-molecular-weight substrate proxies at sites spanning 38 • S to 10 • N in the Atlantic Ocean, and at six depths ranging from surface to bottom water. In surface to upper mesopelagic waters, the spectrum of substrates hydrolyzed followed distinct patterns, with hydrolytic assemblages more similar vertically within a single station than at similar depths across multiple stations. Additionally, the proportion of total hydrolysis occurring above the pycnocline, and the spectrum of substrates hydrolyzed in mesopelagic and deep waters, was positively related to the strength of stratification at a site, while other physichochemical parameters were generally poor predictors of the measured hydrolysis rates. Spatial as well as depth-driven constraints on heterotrophic hydrolytic capacities result in broad variations in potential carbon-degrading activity in the ocean. The spectrum of enzymatic capabilities and rates of hydrolysis in the ocean, and the proportion of organic carbon hydrolyzed above the permanent thermocline, may influence the efficiency of the biological pump and net carbon export across distinct latitudinal and depth regions.

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Niches of two polysaccharide-degrading Polaribacter isolates from the North Sea during a spring diatom bloom

Cited by 169 publications

References 78 publications

Nitrogen fixation in a chemoautotrophic lucinid symbiosis

Nitrogen fixation in a chemoautotrophic lucinid symbiosis

Isolation and Complete Genome Sequence of Algibacter alginolytica sp. nov., a Novel Seaweed-Degrading Bacteroidetes Bacterium with Diverse Putative Polysaccharide Utilization Loci

Heterotrophic Extracellular Enzymatic Activities in the Atlantic Ocean Follow Patterns Across Spatial and Depth Regimes

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