Publications by authors named "Markus Weinbauer"

36 Publications

Viral Lysis Alters the Optical Properties and Biological Availability of Dissolved Organic Matter Derived from Picocyanobacteria.

Appl Environ Microbiol 2021 01 15;87(3). Epub 2021 Jan 15.

State Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Fujian Key Laboratory of Marine Carbon Sequestration, Xiamen University, Xiamen, China

Phytoplankton contribute almost half of the world's total primary production. The exudates and viral lysates of phytoplankton are two important forms of dissolved organic matter (DOM) in aquatic environments and fuel heterotrophic prokaryotic metabolism. However, the effect of viral infection on the composition and biological availability of phytoplankton-released DOM is poorly understood. Here, we investigated the optical characteristics and microbial utilization of the exudates and viral lysates of the ecologically important unicellular picophytoplankton Our results showed that DOM produced by viral lysis (Pro-vDOM) with phages of three different morphotypes (myovirus P-HM2, siphovirus P-HS2, and podovirus P-SSP7) had higher humic-like fluorescence intensities, lower absorption coefficients, and higher spectral slopes than DOM exuded by (Pro-exudate). The results indicate that viral infection altered the composition of -derived DOM and might contribute to the pool of oceanic humic-like DOM. Incubation with Pro-vDOM resulted in a greater dissolved organic carbon (DOC) degradation rate and lower absorption spectral slope and heterotrophic bacterial growth rate than incubation with Pro-exudate, suggesting that Pro-vDOM was more bioavailable than Pro-exudate. In addition, the stimulated microbial community succession trajectories were significantly different between the Pro-exudate and Pro-vDOM treatments, indicating that viral lysates play an important role in shaping the heterotrophic bacterial community. Our study demonstrated that viral lysis altered the chemical composition and biological availability of DOM derived from , which is the numerically dominant phytoplankton in the oligotrophic ocean. The unicellular picocyanobacterium is the numerically dominant phytoplankton in the oligotrophic ocean, contributing to the vast majority of marine primary production. releases a significant fraction of fixed organic matter into the surrounding environment and supports a vital portion of heterotrophic bacterial activity. Viral lysis is an important biomass loss process of However, little is known about whether and how viral lysis affects -released dissolved organic matter (DOM). Our paper shows that viral infection alters the optical properties (such as the absorption coefficients, spectral slopes, and fluorescence intensities) of released DOM and might contribute to a humic-like DOM pool and carbon sequestration in the ocean. Meanwhile, viral lysis also releases various intracellular labile DOM, including amino acids, protein-like DOM, and lower-molecular-weight DOM, increases the bioavailability of DOM, and shapes the successive trajectory of the heterotrophic bacterial community. Our study highlights the importance of viruses in impacting the DOM quality in the ocean.
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http://dx.doi.org/10.1128/AEM.02271-20DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7848921PMC
January 2021

Aquatic Viruses and Climate Change.

Curr Issues Mol Biol 2021 13;41:357-380. Epub 2020 Sep 13.

University of Vienna, Faculty of Life Sciences, Functional and Evolutionary Ecology, Limnology Unit, Vienna, Austria.

The viral component in aquatic systems clearly needs to be incorporated into future ocean and inland water climate models. Viruses have the potential to influence carbon and nutrient cycling in aquatic ecosystems significantly. Changing climate likely has both direct and indirect influence on virus-mediated processes, among them an impact on food webs, biogeochemical cycles and on the overall metabolic performance of whole ecosystems. Here we synthesise current knowledge on potential climate-related consequences for viral assemblages, virus-host interactions and virus functions, and in turn, viral processes contributing to climate change. There is a need to increase the accuracy of predictions of climate change impacts on virus- driven processes, particularly of those linked to biological production and biogeochemical cycles. Comprehension of the relationships between microbial/viral processes and global phenomena is essential to predict the influence on as well as the response of the biosphere to global change.
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http://dx.doi.org/10.21775/cimb.041.357DOI Listing
September 2021

Viral control of biomass and diversity of bacterioplankton in the deep sea.

Commun Biol 2020 05 22;3(1):256. Epub 2020 May 22.

State Key Laboratory of Marine Environmental Science, Fujian Key Laboratory of Marine Carbon Sequestration, College of Ocean and Earth Sciences, Xiamen University (Xiang'an), 361102, Xiamen, Fujian, China.

Viral abundance in deep-sea environments is high. However, the biological, ecological and biogeochemical roles of viruses in the deep sea are under debate. In the present study, microcosm incubations of deep-sea bacterioplankton (2,000 m deep) with normal and reduced pressure of viral lysis were conducted in the western Pacific Ocean. We observed a negative effect of viruses on prokaryotic abundance, indicating the top-down control of bacterioplankton by virioplankton in the deep-sea. The decreased bacterial diversity and a different bacterial community structure with diluted viruses indicate that viruses are sustaining a diverse microbial community in deep-sea environments. Network analysis showed that relieving viral pressure decreased the complexity and clustering coefficients but increased the proportion of positive correlations for the potentially active bacterial community, which suggests that viruses impact deep-sea bacterioplankton interactions. Our study provides experimental evidences of the crucial role of viruses in microbial ecology and biogeochemistry in deep-sea ecosystems.
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http://dx.doi.org/10.1038/s42003-020-0974-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7244761PMC
May 2020

Effects of elevated pCO2 and feeding on net calcification and energy budget of the Mediterranean cold-water coral Madrepora oculata.

J Exp Biol 2016 10 28;219(Pt 20):3208-3217. Epub 2016 Jul 28.

Sorbonne Universités, UPMC Université Paris 06, Observatoire Océanologique de Villefranche, Villefranche-sur-mer 06230, France.

Ocean acidification is a major threat to calcifying marine organisms such as deep-sea cold-water corals (CWCs), but related knowledge is scarce. The aragonite saturation threshold (Ω) for calcification, respiration and organic matter fluxes were investigated experimentally in the Mediterranean Madrepora oculata Over 10 weeks, colonies were maintained under two feeding regimes (uptake of 36.75 and 7.46 µmol C polyp week) and exposed in 2 week intervals to a consecutively changing air-CO mix (pCO) of 400, 1600, 800, 2000 and 400 ppm. There was a significant effect of feeding on calcification at initial ambient pCO, while with consecutive pCO treatments, feeding had no effect on calcification. Respiration was not significantly affected by feeding or pCO levels. Coral skeletons started to dissolve at an average Ω threshold of 0.92, but recovered and started to calcify again at Ω≥1. The surplus energy required to counteract dissolution at elevated pCO (≥1600 µatm) was twice that at ambient pCO Yet, feeding had no mitigating effect at increasing pCO levels. This could be due to the fact that the energy required for calcification is a small fraction (1-3%) of the total metabolic energy demand and corals even under low food conditions might therefore still be able to allocate this small portion of energy to calcification. The response and resistance to ocean acidification are consequently not controlled by feeding in this species, but more likely by chemical reactions at the site of calcification and exchange processes between the calicoblastic layer and ambient seawater.
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http://dx.doi.org/10.1242/jeb.127159DOI Listing
October 2016

Colonization and release processes of viruses and prokaryotes on artificial marine macroaggregates.

FEMS Microbiol Lett 2016 Jan 13;363(1):fnv216. Epub 2015 Nov 13.

CNRS, UMR 7093, LOV, Observatoire Océanologique, 06230 Villefranche-sur-Mer, France Sorbonne Universités, UPMC, Université Paris 06, UMR 7093, LOV, Observatoire Océanologique, 06230 Villefranche-sur-Mer, France Aix Marseille Université, CNRS/INSU, Université de Toulon, IRD, Mediterranean Institute of Oceanography (MIO) UM 110, 13288, Marseille, France.

Marine organic aggregates are sites of high of viral accumulation; however, still little is known about their colonization processes and interactions with their local bacterial hosts. By taking advantage of a novel approach (paramagnetic functionalized microsphere method) to create and incubate artificial macroaggregates, we examined the small-scale movements of viruses and bacteria between such marine snow particles and the surrounding water. The examination of the codynamics of both free-living and attached viral and bacterial abundance, over 12 hours of incubation in virus-free water, suggests that aggregates are rather comparable to viral factories than to viral traps where a significant part of the virions production might be locally diverted to the water column. Also, the near-zero proportion of lysogenized cells measured in aggregates after mitomycin-C induction seems to indicate that lysogeny is not a prominent viral reproduction pathway in organic aggregates where most viruses might rather be virulent. Finally, we hypothesize that, contrary to bacteria, which can use both strong attachment and detachment from aggregates (two-way motion of bacteria), the adsorption of planktonic viruses appears to be numerically negligible compared to their massive export from the aggregates into the water column (one-way motion of viruses).
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http://dx.doi.org/10.1093/femsle/fnv216DOI Listing
January 2016

Comparison of deep-water viromes from the atlantic ocean and the mediterranean sea.

PLoS One 2014 24;9(6):e100600. Epub 2014 Jun 24.

Department of Limnology and Oceanography, University of Vienna, Vienna, Austria; Department of Biological Oceanography, Royal Netherlands Institute for Sea Research, Den Burg, The Netherlands.

The aim of this study was to compare the composition of two deep-sea viral communities obtained from the Romanche Fracture Zone in the Atlantic Ocean (collected at 5200 m depth) and the southwest Mediterranean Sea (from 2400 m depth) using a pyro-sequencing approach. The results are based on 18.7% and 6.9% of the sequences obtained from the Atlantic Ocean and the Mediterranean Sea, respectively, with hits to genomes in the non-redundant viral RefSeq database. The identifiable richness and relative abundance in both viromes were dominated by archaeal and bacterial viruses accounting for 92.3% of the relative abundance in the Atlantic Ocean and for 83.6% in the Mediterranean Sea. Despite characteristic differences in hydrographic features between the sampling sites in the Atlantic Ocean and the Mediterranean Sea, 440 virus genomes were found in both viromes. An additional 431 virus genomes were identified in the Atlantic Ocean and 75 virus genomes were only found in the Mediterranean Sea. The results indicate that the rather contrasting deep-sea environments of the Atlantic Ocean and the Mediterranean Sea share a common core set of virus types constituting the majority of both virus communities in terms of relative abundance (Atlantic Ocean: 81.4%; Mediterranean Sea: 88.7%).
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0100600PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4069082PMC
March 2015

Interactive effects of viral and bacterial production on marine bacterial diversity.

PLoS One 2013 7;8(11):e76800. Epub 2013 Nov 7.

Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba, Japan ; Center for Ecological Research, Kyoto University, Otsu, Shiga, Japan ; Université Pierre et Marie Curie-Paris 6, Laboratoire d'Océanographie de Villefranche, Villefranche-sur-Mer, France ; CNRS, Laboratoire d'Océanographie de Villefranche, Villefranche-sur-Mer, France.

A general model of species diversity predicts that the latter is maximized when productivity and disturbance are balanced. Based on this model, we hypothesized that the response of bacterial diversity to the ratio of viral to bacterial production (VP/BP) would be dome-shaped. In order to test this hypothesis, we obtained data on changes in bacterial communities (determined by terminal restriction fragment length polymorphism of 16S rRNA gene) along a wide VP/BP gradient (more than two orders of magnitude), using seawater incubations from NW Mediterranean surface waters, i.e., control and treatments with additions of phosphate, viruses, or both. In December, one dominant Operational Taxonomic Unit accounted for the major fraction of total amplified DNA in the phosphate addition treatment (75±20%, ± S.D.), but its contribution was low in the phosphate and virus addition treatment (23±19%), indicating that viruses prevented the prevalence of taxa that were competitively superior in phosphate-replete conditions. In contrast, in February, the single taxon predominance in the community was held in the phosphate addition treatment even with addition of viruses. We observed statistically robust dome-shaped response patterns of bacterial diversity to VP/BP, with significantly high bacterial diversity at intermediate VP/BP. This was consistent with our model-based hypothesis, indicating that bacterial production and viral-induced mortality interactively affect bacterial diversity in seawater.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0076800PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3820650PMC
July 2014

End of the century pCO₂ levels do not impact calcification in Mediterranean cold-water corals.

PLoS One 2013 30;8(4):e62655. Epub 2013 Apr 30.

Centre National de la Recherche Scientifique-Institut National des Sciences de l'Univers, Laboratoire d'Océanographie de Villefranche, Villefranche-sur-mer, France.

Ocean acidification caused by anthropogenic uptake of CO₂ is perceived to be a major threat to calcifying organisms. Cold-water corals were thought to be strongly affected by a decrease in ocean pH due to their abundance in deep and cold waters which, in contrast to tropical coral reef waters, will soon become corrosive to calcium carbonate. Calcification rates of two Mediterranean cold-water coral species, Lophelia pertusa and Madrepora oculata, were measured under variable partial pressure of CO₂ (pCO₂) that ranged between 380 µatm for present-day conditions and 930 µatm for the end of the century. The present study addressed both short- and long-term responses by repeatedly determining calcification rates on the same specimens over a period of 9 months. Besides studying the direct, short-term response to elevated pCO₂ levels, the study aimed to elucidate the potential for acclimation of calcification of cold-water corals to ocean acidification. Net calcification of both species was unaffected by the levels of pCO₂ investigated and revealed no short-term shock and, therefore, no long-term acclimation in calcification to changes in the carbonate chemistry. There was an effect of time during repeated experiments with increasing net calcification rates for both species, however, as this pattern was found in all treatments, there is no indication that acclimation of calcification to ocean acidification occurred. The use of controls (initial and ambient net calcification rates) indicated that this increase was not caused by acclimation in calcification response to higher pCO₂. An extrapolation of these data suggests that calcification of these two cold-water corals will not be affected by the pCO₂ level projected at the end of the century.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0062655PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3640017PMC
November 2013

Response of bacterioplankton to a glucose gradient in the absence of lysis and grazing.

FEMS Microbiol Ecol 2013 Sep 1;85(3):443-51. Epub 2013 May 1.

State Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen, China.

Bacterial utilization of dissolved organic matter plays an important role in marine carbon cycling. In this study, the response of bacterioplankton to a gradient of carbon (glucose) addition was investigated experimentally in a subtropical coastal environment in the absence of top-down control by viruses and flagellates. Bacterial abundance and production were stimulated by glucose addition corresponding to a gradient of glucose. Differences in the extent of stimulation suggested different bacterial life strategies under different nutrient conditions. Bacterial community diversity as revealed by denaturing gradient gel electrophoresis (DGGE) showed a unimodal productivity-diversity (number of DGGE bands) relationship after 3-day incubation. DNA fingerprinting profiling and cluster analysis showed clear and gradual changes in bacterial community structure along the gradient of glucose concentrations, reflecting the competition for carbon supply among bacterial groups. Sequencing analysis of the DGGE bands disclosed the relative abundance of seven bacterial genotypes in the Alteromonadaceae and Roseovarius that gradually decreased with the glucose enrichment while two Vibrio genotypes showed the reverse increasing trend. This suggested that Vibrio was a more successful opportunist at high carbon availability.
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http://dx.doi.org/10.1111/1574-6941.12133DOI Listing
September 2013

Effects of sodium azide on the abundance of prokaryotes and viruses in marine samples.

PLoS One 2012 18;7(5):e37597. Epub 2012 May 18.

Department of Marine Biology, University of Vienna, Vienna, Austria.

Flow cytometry is set to become the standard method for enumerating prokaryotes and viruses in marine samples. However, the samples need to be flash-frozen in liquid nitrogen directly after aldehyde fixation. Because liquid nitrogen may not always be available, we tested the potential of sodium azide as a preservative for prokaryotes and viruses in marine samples as a possible alternative. For that we conducted incubation experiments with untreated and sodium azide treated marine water samples at 4°C and room temperature. The data indicate that sodium azide cannot be used to maintain marine samples used for the enumeration of prokaryotes and viruses.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0037597PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3356311PMC
September 2012

Development of phoH as a novel signature gene for assessing marine phage diversity.

Appl Environ Microbiol 2011 Nov 16;77(21):7730-9. Epub 2011 Sep 16.

College of Marine Science, University of South Florida, St. Petersburg, FL 33701, USA.

Phages play a key role in the marine environment by regulating the transfer of energy between trophic levels and influencing global carbon and nutrient cycles. The diversity of marine phage communities remains difficult to characterize because of the lack of a signature gene common to all phages. Recent studies have demonstrated the presence of host-derived auxiliary metabolic genes in phage genomes, such as those belonging to the Pho regulon, which regulates phosphate uptake and metabolism under low-phosphate conditions. Among the completely sequenced phage genomes in GenBank, this study identified Pho regulon genes in nearly 40% of the marine phage genomes, while only 4% of nonmarine phage genomes contained these genes. While several Pho regulon genes were identified, phoH was the most prevalent, appearing in 42 out of 602 completely sequenced phage genomes. Phylogenetic analysis demonstrated that phage phoH sequences formed a cluster distinct from those of their bacterial hosts. PCR primers designed to amplify a region of the phoH gene were used to determine the diversity of phage phoH sequences throughout a depth profile in the Sargasso Sea and at six locations worldwide. phoH was present at all sites examined, and a high diversity of phoH sequences was recovered. Most phoH sequences belonged to clusters without any cultured representatives. Each depth and geographic location had a distinct phoH composition, although most phoH clusters were recovered from multiple sites. Overall, phoH is an effective signature gene for examining phage diversity in the marine environment.
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http://dx.doi.org/10.1128/AEM.05531-11DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3209181PMC
November 2011

A preliminary study on metal and nutrient concentrations in running water systems in southern New Caledonia.

Bull Environ Contam Toxicol 2011 Oct 24;87(4):361-5. Epub 2011 Jul 24.

Laboratoire d'Océanographie de Villefranche, Université Pierre et Marie Curie, UMR 7093, 06230 Villefranche-sur-Mer, France.

Metal and nutrient concentrations were measured in five running water sampling sites of New Caledonia. Metal concentrations were homogeneous (Ni; 22.7-50.6 μg L(-1)) or not (Fe; 37-749 μg L(-1)). Concentrations of Ni, Cr, Fe were high, including high dissolved fractions (up to 47.8, 70.8 and 417 μg L(-1), respectively). Concentrations of anthropogenic metals (Ag, As, Cd, Cu, Pb, Sb, V, Zn) were low (maximum: total Cu, 0.6 μg L(-1)). The contamination of waters is presumably due to soil weathering and mining activities. Metal concentrations and phosphate depletion (<0.04 μmol L(-1)) suggest constrained conditions for the development of aquatic life.
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http://dx.doi.org/10.1007/s00128-011-0367-zDOI Listing
October 2011

Association of marine viral and bacterial communities with reference black carbon particles under experimental conditions: an analysis with scanning electron, epifluorescence and confocal laser scanning microscopy.

FEMS Microbiol Ecol 2010 Nov 3;74(2):382-96. Epub 2010 Aug 3.

Laboratoire d'Océanographie de Villefranche, Microbial Ecology & Biogeochemistry Group, Université Pierre et Marie Curie-Paris 6, Villefranche-sur-Mer, France.

Black carbon (BC), the product of incomplete combustion of fossil fuels and biomass, constitutes a significant fraction of the marine organic carbon pool. However, little is known about the possible interactions of BC and marine microorganisms. Here, we report the results of experiments using a standard reference BC material in high concentrations to investigate basic principles of the dynamics of natural bacterial and viral communities with BC particles. We assessed the attachment of viral and bacterial communities using scanning electron, epifluorescence and confocal laser scanning microscopy and shifts in bacterial community composition using 16S rRNA gene denaturing gradient gel electrophoresis (DGGE). In 24-h time-course experiments, BC particles showed a strong potential for absorbing viruses and bacteria. Total viral abundance was reduced, whereas total bacterial abundance was stimulated in the BC treatments. Viral and bacterial abundance on BC particles increased with particle size, whereas the abundances of BC-associated viruses and bacteria per square micrometer surface area decreased significantly with BC particle size. DGGE results suggested that BC has the potential to change bacterial community structure and favour phylotypes related to Glaciecola sp. Our study indicates that BC could influence processes mediated by bacteria and viruses in marine ecosystems.
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http://dx.doi.org/10.1111/j.1574-6941.2010.00953.xDOI Listing
November 2010

Randomly amplified polymorphic DNA reveals tight links between viruses and microbes in the bathypelagic zone of the Northwestern Mediterranean Sea.

Appl Environ Microbiol 2010 Oct 20;76(20):6724-32. Epub 2010 Aug 20.

Department of Marine Biology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria.

The study site located in the Mediterranean Sea was visited eight times in 2005 and 2006 to collect samples from the epipelagic (5 m), mesopelagic (200 m, 600 m), and bathypelagic (1,000 m, 2,000 m) zones. Randomly amplified polymorphic DNA PCR (RAPD-PCR) analysis was used to obtain fingerprints from microbial and viral size fractions using two different primers each. Depending on the primer used, the number of bands in the water column varied between 12 to 24 and 6 to 19 for the microbial size fraction and between 16 to 26 and 8 to 22 for the viral size fraction. The majority of sequences from the microbial fraction was related to Alphaproteobacteria, Cyanobacteria, Gammaproteobacteria, Firmicutes, and Eukaryota. Only 9% of sequences obtained from the viral fraction were of identifiable viral origin; however, 76% of sequences had no close relatives in the nr database of GenBank. Only 20.1% of complete phage genomes tested in silico resulted in potential RAPD-PCR products, and only 12% of these were targeted by both primers. Also, in silico analysis indicated that RAPD-PCR profiles obtained by the two different primers are largely representative of two different subsets of the viral community. Also, correlation analyses and Mantel tests indicate that the links between changes in the microbial and viral community were strongest in the bathypelagic. Thus, these results suggest a strong codevelopment of virus and host communities in deep waters. The data also indicate that virus communities in the bathypelagic zone can exhibit substantial temporal dynamics.
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http://dx.doi.org/10.1128/AEM.00531-10DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2953038PMC
October 2010

Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean.

Nat Rev Microbiol 2010 Aug 5;8(8):593-9. Epub 2010 Jul 5.

State Key Laboratory of Marine Environmental Sciences, Xiamen University, 361005, China.

The biological pump is a process whereby CO(2) in the upper ocean is fixed by primary producers and transported to the deep ocean as sinking biogenic particles or as dissolved organic matter. The fate of most of this exported material is remineralization to CO(2), which accumulates in deep waters until it is eventually ventilated again at the sea surface. However, a proportion of the fixed carbon is not mineralized but is instead stored for millennia as recalcitrant dissolved organic matter. The processes and mechanisms involved in the generation of this large carbon reservoir are poorly understood. Here, we propose the microbial carbon pump as a conceptual framework to address this important, multifaceted biogeochemical problem.
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http://dx.doi.org/10.1038/nrmicro2386DOI Listing
August 2010

Trade-offs between competition and defense specialists among unicellular planktonic organisms: the "killing the winner" hypothesis revisited.

Microbiol Mol Biol Rev 2010 Mar;74(1):42-57

University of Vienna, Faculty of Life Sciences, Department of Marine Biology, Althanstrasse 14, 1090 Vienna, Austria.

A trade-off between strategies maximizing growth and minimizing losses appears to be a fundamental property of evolving biological entities existing in environments with limited resources. In the special case of unicellular planktonic organisms, the theoretical framework describing the trade-offs between competition and defense specialists is known as the "killing the winner" hypothesis (KtW). KtW describes how the availability of resources and the actions of predators (e.g., heterotrophic flagellates) and parasites (e.g., viruses) determine the composition and biogeochemical impact of such organisms. We extend KtW conceptually by introducing size- or shape-selective grazing of protozoans on prokaryotes into an idealized food web composed of prokaryotes, lytic viruses infecting prokaryotes, and protozoans. This results in a hierarchy analogous to a Russian doll, where KtW principles are at work on a lower level due to selective viral infection and on an upper level due to size- or shape-selective grazing by protozoans. Additionally, we critically discuss predictions and limitations of KtW in light of the recent literature, with particular focus on typically neglected aspects of KtW. Many aspects of KtW have been corroborated by in situ and experimental studies of isolates and natural communities. However, a thorough test of KtW is still hampered by current methodological limitations. In particular, the quantification of nutrient uptake rates of the competing prokaryotic populations and virus population-specific adsorption and decay rates appears to be the most daunting challenge for the years to come.
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http://dx.doi.org/10.1128/MMBR.00034-09DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2832346PMC
March 2010

Assessing niche separation among coexisting Limnohabitans strains through interactions with a competitor, viruses, and a bacterivore.

Appl Environ Microbiol 2010 Mar 28;76(5):1406-16. Epub 2009 Dec 28.

Biology Centre of the Academy of Sciences of the Czech Republic, Hydrobiological Institute, Ceské Budejovice, Czech Republic.

We investigated potential niche separation in two closely related (99.1% 16S rRNA gene sequence similarity) syntopic bacterial strains affiliated with the R-BT065 cluster, which represents a subgroup of the genus Limnohabitans. The two strains, designated B4 and D5, were isolated concurrently from a freshwater reservoir. Differences between the strains were examined through monitoring interactions with a bacterial competitor, Flectobacillus sp. (FL), and virus- and predator-induced mortality. Batch-type cocultures, designated B4+FL and D5+FL, were initiated with a similar biomass ratio among the strains. The proportion of each cell type present in the cocultures was monitored based on clear differences in cell sizes. Following exponential growth for 28 h, the cocultures were amended by the addition of two different concentrations of live or heat-inactivated viruses concentrated from the reservoir. Half of virus-amended treatments were inoculated immediately with an axenic flagellate predator, Poterioochromonas sp. The presence of the predator, of live viruses, and of competition between the strains significantly affected their population dynamics in the experimentally manipulated treatments. While strains B4 and FL appeared vulnerable to environmental viruses, strain D5 did not. Predator-induced mortality had the greatest impact on FL, followed by that on D5 and then B4. The virus-vulnerable B4 strain had smaller cells and lower biomass yield, but it was less subject to grazing. In contrast, the seemingly virus-resistant D5, with slightly larger grazing-vulnerable cells, was competitive with FL. Overall, our data suggest contrasting ecophysiological capabilities and partial niche separation in two coexisting Limnohabitans strains.
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http://dx.doi.org/10.1128/AEM.02517-09DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2832377PMC
March 2010

Viral control of bacterial biodiversity--evidence from a nutrient-enriched marine mesocosm experiment.

Environ Microbiol 2009 Oct 24;11(10):2585-97. Epub 2009 Jun 24.

University of Bergen, PO Box 7800, Department of Biology, N-5020 Bergen, Norway.

We demonstrate here results showing that bottom-up and top-down control mechanisms can operate simultaneously and in concert in marine microbial food webs, controlling prokaryote diversity by a combination of viral lysis and substrate limitation. Models in microbial ecology predict that a shift in the type of bacterial growth rate limitation is expected to have a major effect on species composition within the community of bacterial hosts, with a subsequent shift in the composition of the viral community. Only moderate effects would, however, be expected in the absolute number of coexisting virus-host pairs. We investigated these relationships in nutrient-manipulated systems, under simulated in situ conditions. There was a strong correlation in the clustering of the viral and bacterial community data supporting the existence of an important link between the bacterial and viral communities. As predicted, the total number of viral populations was the same in all treatments, while the composition of the viral community varied. Our results support the theoretical prediction that there is one control mechanism for the number of niches for coexisting virus-host pairs (top-down control), and another mechanism that controls which virus-host pairs occupy these niches (bottom-up control).
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http://dx.doi.org/10.1111/j.1462-2920.2009.01983.xDOI Listing
October 2009

Viral and flagellate control of prokaryotic production and community structure in offshore Mediterranean waters.

Appl Environ Microbiol 2009 Jul 22;75(14):4801-12. Epub 2009 May 22.

CNRS UMR 7093, Laboratoire d'Océanographie de Villefranche, BP 28, 06234 Villefranche-sur-Mer Cedex, France.

A dilution and size fractionation approach was used to study the separate and combined effects of viruses and flagellates on prokaryotic production ([(3)H]leucine incorporation) and community composition (16S rRNA gene PCR and denaturing gradient gel electrophoresis [DGGE]) in the upper mixed layer and the deep chlorophyll maximum in the offshore Mediterranean Sea. Four experiments were established using differential filtration: a resource control without predators (C treatment), treatment in the presence of viruses (V treatment), treatment in the presence of flagellates (F treatment), and treatment in the presence of both predators (VF treatment). The V and VF treatments increased prokaryotic abundance (1.4- to 2.3-fold) and the number of DGGE bands (by up to 43%) and decreased prokaryotic production compared to the level for the C treatment (by 22 to 99%). For the F treatment, significant differences compared to the level for the C treatment were found as well, but trends were not consistent across experiments. The relative abundances of the high-nucleic-acid subgroups of prokaryotes with high scatter (HNAhs) in flow cytometer settings were lower in the V and VF treatments than in the C and F treatments. These differences were probably due to lysis of very active HNA prokaryotes in the V and VF treatments. Our results indicate that the presence of viruses or viruses plus flagellates sustains prokaryotic diversity and controls prokaryotic production by regulating the proportion of the highly active members of the community. Our data also suggest that lysis and grazing control influences the relationship between bacterial community composition and prokaryotic production.
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http://dx.doi.org/10.1128/AEM.01376-08DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2708420PMC
July 2009

Annual changes of bacterial mortality due to viruses and protists in an oligotrophic coastal environment (NW Mediterranean).

Environ Microbiol 2009 May;11(5):1181-93

Institut de Ciències del Mar (CSIC), Barcelona, Spain.

The impact of viruses and protists on bacterioplankton mortality was examined monthly during 2 years (May 2005-April 2007) in an oligotrophic coastal environment (NW Mediterranean Sea). We expected that in such type of system, (i) bacterial losses would be caused mainly by protists, and (ii) lysogeny would be an important type of virus-host interaction. During the study period, viruses and grazers together were responsible for 50.6 +/- 40.1% day(-1) of bacterial standing stock losses (BSS) and 59.7 +/- 44.0% day(-1) of bacterial production losses (BP). Over the first year (May 2005-April 2006), protists were the principal cause of bacterial mortality, removing 29.9 +/- 20.4% day(-1) of BSS and 33.9 +/- 24.3% day(-1) of BP, whereas viral lysis removed 13.5 +/- 17.0% day(-1) of BSS and 12.3 +/- 12.3% day(-1) of BP. During the second year (May 2006-April 2007), viruses caused comparable bacterial losses (29.2 +/- 14.8% day(-1) of BSS and 40.9 +/- 20.7% day(-1) of BP) to protists (28.6 +/- 25.5% day(-1) of BSS and 32.4 +/- 20.0% day(-1) of BP). In 37% of cases higher losses of BP due to viruses than due to protists were found. Lysogenic infection was detected in 11 of 24 samplings. Contrary to our expectations, lytic infections dominated over the two years, and viruses resulted to be a significant source of bacterial mortality in this oligotrophic site.
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http://dx.doi.org/10.1111/j.1462-2920.2008.01849.xDOI Listing
May 2009

Major viral impact on the functioning of benthic deep-sea ecosystems.

Nature 2008 Aug;454(7208):1084-7

Department of Marine Science, Faculty of Science, Polytechnic University of Marche, Via Brecce Bianche, 60131 Ancona, Italy.

Viruses are the most abundant biological organisms of the world's oceans. Viral infections are a substantial source of mortality in a range of organisms-including autotrophic and heterotrophic plankton-but their impact on the deep ocean and benthic biosphere is completely unknown. Here we report that viral production in deep-sea benthic ecosystems worldwide is extremely high, and that viral infections are responsible for the abatement of 80% of prokaryotic heterotrophic production. Virus-induced prokaryotic mortality increases with increasing water depth, and beneath a depth of 1,000 m nearly all of the prokaryotic heterotrophic production is transformed into organic detritus. The viral shunt, releasing on a global scale approximately 0.37-0.63 gigatonnes of carbon per year, is an essential source of labile organic detritus in the deep-sea ecosystems. This process sustains a high prokaryotic biomass and provides an important contribution to prokaryotic metabolism, allowing the system to cope with the severe organic resource limitation of deep-sea ecosystems. Our results indicate that viruses have an important role in global biogeochemical cycles, in deep-sea metabolism and the overall functioning of the largest ecosystem of our biosphere.
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http://dx.doi.org/10.1038/nature07268DOI Listing
August 2008

Dynamics and diversity of newly produced virioplankton in the North Sea.

ISME J 2008 Sep 12;2(9):924-36. Epub 2008 Jun 12.

Department of Biological Oceanography, Royal Netherlands Institute for Sea Research, Texel, The Netherlands.

Viral diversity has been studied in a variety of marine habitats and spatial and seasonal changes have been documented. Most of the bacteriophages are considered host specific and are thought to affect fast growing prokaryotic phylotypes more than slow growing ones. We hypothesized that viral infection and consequently, lysis occurs in pulses with only a few prokaryotic phylotypes lysed at any given time. Thus, we propose that the newly produced viruses represent only a fraction of the viral diversity present at any given time. Virioplankton diversity was assessed by pulsed-field gel electrophoresis in the surface waters of three distinct areas of the North Sea during the spring and summer. Bulk virioplankton diversity was fairly stable in these waters. Viral diversity produced by the indigenous bacterioplankton, however, exhibited day-to-day variability with only a few bands produced at any given time. These bands frequently matched bands of the in situ virioplankton; however, bands not present in the band pattern of the in situ virioplankton community were also found. These new bands probably indicate infection and subsequent release of viruses from bacterioplankton phylotypes previously not infected by these specific viruses. Overall, our results demonstrate that viral infection and lysis are rather dynamic processes. The main targets of viral infection are changing apparently on time scales of hours to days indicating that viral infection might effectively regulate and maintain bacterioplankton diversity.
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http://dx.doi.org/10.1038/ismej.2008.57DOI Listing
September 2008

Relationship of geographic distance, depth, temperature, and viruses with prokaryotic communities in the eastern tropical Atlantic Ocean.

Microb Ecol 2008 Aug 7;56(2):383-9. Epub 2007 Dec 7.

University of British Columbia, EOS-Oceanography, Vancouver, BC V6T 1Z4, Canada.

The richness and biogeographical distribution pattern of bacterial and archaeal communities was assessed by terminal restriction fragment length polymorphism analysis of polymerase chain reaction-amplified fragments of the 16S rRNA gene at the surface (15-25 m depth), in the deep chlorophyll maximum layer (DCM; 50 m depth), and deep waters (75-1000 m depth) of the eastern tropical Atlantic Ocean. Additionally, prokaryotic and viral abundance and the frequency of infected prokaryotic cells (FIC) were determined along with physico-chemical parameters to identify factors influencing prokaryotic richness and biogeography. Viral abundance was highest in the DCM layer averaging 45.5 x 10(6) ml(-1), whereas in the mixed surface layer and in the waters below the DCM, average viral abundance was 11.3 x 10(6) and 4.3 x 10(6) ml(-1), respectively. The average estimate of FIC was 8.3% in the mixed surface layer and the DCM and 2.4% in deeper waters. FIC was positively related to prokaryotic and viral abundance and negatively to archaeal richness. There was no detectable effect of geographic distance (maximum distance between stations approximately 4600 km) or differences between water masses on bacterial and archaeal community composition. Bacterial communities showed a clear depth zonation, whereas changes in archaeal community composition were related to temperature and FIC. The results indicate that planktonic archaeal virus host systems are a dynamic component of marine ecosystems under natural conditions.
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http://dx.doi.org/10.1007/s00248-007-9343-xDOI Listing
August 2008

Viruses and flagellates sustain apparent richness and reduce biomass accumulation of bacterioplankton in coastal marine waters.

Environ Microbiol 2007 Dec;9(12):3008-18

Department of Biology and Coastal Marine Laboratory, The Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, Hong Kong, China.

To gain a better understanding of the interactions among bacteria, viruses and flagellates in coastal marine ecosystems, we investigated the effect of viral lysis and protistan bacterivory on bacterial abundance, production and diversity [determined by 16S rRNA gene polymerase chain reaction (PCR) and denaturing gradient gel electrophoresis (DGGE)] in three coastal marine sites with different nutrient supplies in Hong Kong. Six experiments were set up using filtration and dilution methods to develop virus, flagellate and virus+flagellate treatments for natural bacterial populations. All three predation treatments had significant repressing effects on bacterial abundance. Bacterial production was significantly repressed by flagellates and both predators (flagellates and viruses). Bacterial apparent species richness (indicated as the number of DGGE bands) was always significantly higher in the presence of viruses, flagellates and both predators than in the predator-free control. Cluster analysis of the DGGE patterns showed that the effects of viruses and flagellates on bacterial community structure were relatively stochastic while the co-effects of predators caused consistent trends (DGGE always showed the most similar patterns when compared with those of in situ environments) and substantially increased the apparent richness. Overall, we found strong evidence that viral lysis and protist bacterivory act additively to reduce bacterial production and to sustain diversity. This first systematic attempt to study the interactive effects of viruses and flagellates on the diversity and production of bacterial communities in coastal waters suggests that a tight control of bacterioplankton dominants results in relatively stable bacterioplankton communities.
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http://dx.doi.org/10.1111/j.1462-2920.2007.01410.xDOI Listing
December 2007

Virus attachment to transparent exopolymeric particles along trophic gradients in the southwestern lagoon of New Caledonia.

Appl Environ Microbiol 2007 Aug 22;73(16):5245-52. Epub 2007 Jun 22.

IRD, Noumea Center, BP A5, NC-98848 Noumea, New Caledonia.

Viruses on organic aggregates such as transparent exopolymeric particles (TEP) are not well investigated. The number of TEP-attached viruses was assessed along trophic gradients in the southwestern lagoon of New Caledonia by determining the fraction of viruses removed after magnetic isolation of TEP. In order to isolate TEP magnetically, TEP were formed in the presence of magnetic beads from submicrometer precursors collected along the trophic gradients. The mixed aggregates of TEP-beads-viruses were removed from solution with a magnetic field. The percentage of viruses associated with newly formed TEP averaged 8% (range, 3 to 13%) for most of the stations but was higher (ca. 30%) in one bay characterized by the low renewal rate of its water mass. The number of viruses (N) attached to TEP varied as a function of TEP size (d [in micrometers]) according to the formulas N = 100d(1.60) and N = 230d(1.75), respectively, for TEP occurring in water masses with short (i.e., <40 days) and long (i.e., >40 days) residence times. These two relationships imply that viral abundance decreases with TEP size, and they indicate that water residence time influences viral density and virus-bacterium interactions within aggregates. Our data suggest that the fraction of viruses attached to TEP is highest in areas characterized by a low renewal rate of the water mass and can constitute at times a significant fraction of total virus abundance. Due to the small distance between viruses and hosts on TEP, these particles may be hot spots for viral infection.
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http://dx.doi.org/10.1128/AEM.00762-07DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1950989PMC
August 2007

Viral abundance, decay, and diversity in the meso- and bathypelagic waters of the north atlantic.

Appl Environ Microbiol 2007 Jul 11;73(14):4429-38. Epub 2007 May 11.

Department of Biological Oceanography, Royal Netherlands Institute for Sea Research (NIOZ), 1790 AB Den Burg, Texel, The Netherlands.

To elucidate the potential importance of deep-water viruses in controlling the meso- and bathypelagic picoplankton community, the abundance, decay rate, and diversity of the virioplankton community were determined in the meso- and bathypelagic water masses of the eastern part of the subtropical North Atlantic. Viral abundance averaged 1.4 x 10(6) ml(-1) at around 100 m of depth and decreased only by a factor of 2 at 3,000 to 4,000 m of depth. In contrast, picoplankton abundance decreased by 1 order of magnitude to the Lower Deep Water (LDW; 3,500- to 5,000-m depth). The virus-to-picoplankton ratio increased from 9 at about 100 m of depth to 110 in the LDW. Mean viral decay rates were 3.5 x 10(-3) h(-1) between 900 m and 2,750 m and 1.1 x 10(-3) h(-1) at 4,000 m of depth, corresponding to viral turnover times of 11 and 39 days, respectively. Pulsed-field gel electrophoresis fingerprints obtained from the viral community between 2,400 m and 4,000 m of depth revealed a maximum of only four bands from 4,000 m of depth. Based on the high viral abundance and the low picoplankton production determined via leucine incorporation, we conclude that the viral production calculated from the viral decay is insufficient to maintain the high viral abundance in the deep North Atlantic. Rather, we propose that substantial allochthonous viral input or lysogenic or pseudolysogenic production is required to maintain the high viral abundance detected in the meso- and bathypelagic North Atlantic. Consequently, deep-water prokaryotes are apparently far less controlled in their abundance and taxon richness by lytic prokaryotic phages than the high viral abundance and the virus-to-picoplankton ratio would suggest.
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http://dx.doi.org/10.1128/AEM.00029-07DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1932831PMC
July 2007

Grazer and virus-induced mortality of bacterioplankton accelerates development of Flectobacillus populations in a freshwater community.

Environ Microbiol 2007 Mar;9(3):789-800

Biological Centre of the Academy of Sciences of the Czech Republic, Hydrobiological Institute, Na Sádkách 7, CZ-37005 Céské Budéjovice, Czech Republic.

We present a detailed analysis of the effects of distinct bacterial mortality factors, viral lysis and heterotrophic nanoflagellates (HNF) bacterivory, associated with the development of filamentous Flectobacillus populations. Reservoir bacterioplankton communities were subjected to additions of both HNF and viruses together, or HNF alone, and then incubated in situ in dialyses bags. For distinct bacterial groups, mortality or growth stimulation was analysed by examining bacterial prey ingested in HNF food vacuoles with fluorescence in situ hybridization (FISH) and via FISH with microautoradiography (MAR-FISH). We also developed a semi-quantitative MAR-FISH-based estimation of relative activities of Flectobacillus populations (targeted by the R-FL615 probe). Bacterial groups vulnerable to HNF predation (mainly clusters of Betaproteobacteria), or discriminated against (Actinobacteria), were detected. Bacterial lineages most vulnerable to virus-lysis (mainly the Betaproteobacteria not targeted by the R-BT065 probe, of the Polynucleobacter cluster) were identified by comparing treatments with HNF alone to HNF and viruses together. Filaments affiliated with the Flectobacillus cluster appeared in both treatments, but were about twice as abundant, long and active as in incubations with viruses and HNF as compared with HNF alone. Viruses appeared to selectively suppress several bacterial groups, perhaps enhancing substrate availability thus stimulating growth and activity of filamentous Flectobacillus.
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http://dx.doi.org/10.1111/j.1462-2920.2006.01201.xDOI Listing
March 2007

Synergistic and antagonistic effects of viral lysis and protistan grazing on bacterial biomass, production and diversity.

Environ Microbiol 2007 Mar;9(3):777-88

Microbial Ecology and Biogeochemistry Group, Université Pierre et Marie Curie-Paris 6, Laboratoire d'Océanographie de Villefranche, 06230 Villefranche-sur-Mer, France.

In a mesotrophic reservoir, we examined the effects on the bacterioplankton of distinct consumers of bacteria, viruses and heterotrophic nanoflagellates, both alone and combined in an experiment using natural populations and in situ incubations in dialysis bags. Ribosomal RNA-targeted probes were employed as well as 16S RNA gene based PCR denaturing gradient gel electrophoresis (DGGE) to enumerate bacterial groups and assess bacterial community composition. We employed probes for Actinobacteria (HGC69a probe), Cytophaga-Flavobacterium-Bacteroidetes bacteria (CF319a probe), BET42a probe (Betaproteobacteria) and a subgroup-Betaproteobacteria (R-BT065 probe). We found consumer-specific effects on bacterial activity and diversity (against a background of CF and BET dominating all treatments) suggesting distinct vulnerabilities to the two sources of mortality. For example, growth rate of Actinobacteria was only positive in the presence of flagellates, while towards the end of the experiment (T(72-96 h)) growth rate of R-BT was only positive in the viruses only treatment. More specific data on how viruses and flagellates influenced Flectobacillus are shown in the companion paper. Highest richness (number of DGGE bands) was found in the virus only treatment and lowest when both consumers were present. In addition, we found suggestions of both antagonistic and synergistic interactions between the two sources of bacterial mortality. Notably, bactivory by flagellates was associated with reductions in bacterial diversity and increases in viral production.
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http://dx.doi.org/10.1111/j.1462-2920.2006.01200.xDOI Listing
March 2007

Shewanella irciniae sp. nov., a novel member of the family Shewanellaceae, isolated from the marine sponge Ircinia dendroides in the Bay of Villefranche, Mediterranean Sea.

Int J Syst Evol Microbiol 2006 Dec;56(Pt 12):2871-2877

Coastal Marine Laboratory/Department of Biology, The Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, Hong Kong SAR, People's Republic of China.

Strain UST040317-058(T), comprising non-pigmented, rod-shaped, facultatively anaerobic, Gram-negative cells that are motile by means of single polar flagella, was isolated from the surface of a marine sponge (Ircinia dendroides) collected from the Mediterranean Sea. Comparative 16S rRNA gene sequence-based phylogenetic analysis placed the strain in a separate cluster with the recognized bacterium Shewanella algae IAM 14159(T), with which it showed a sequence similarity of 95.0 %. The sequence similarity between strain UST040317-058(T) and its other (six) closest relatives ranged from 91.6 to 93.8 %. Strain UST040317-058(T) showed oxidase, catalase and gelatinase activities. The typical respiratory quinones for shewanellas, menaquinone MK-7 and ubiquinones Q-7 and Q-8, were also detected. The predominant fatty acids in strain UST040317-058(T) were i15 : 0, 16 : 0, 17 : 1omega8c and summed feature 3 (comprising i15 : 0 2-OH and/or 16 : 1omega7c), altogether representing 56.9 % of the total. The DNA G+C content was 39.9 mol%. The strain could be differentiated from other Shewanella species by its inability to reduce nitrate or produce H(2)S and by 10-22 additional phenotypic characteristics. On the basis of the phylogenetic and phenotypic data presented in this study, strain UST040317-058(T) represents a novel species in the genus Shewanella, for which the name Shewanella irciniae sp. nov. is proposed. The type strain is UST040317-058(T) (=JCM 13528(T)=NRRL B-41466(T)).
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http://dx.doi.org/10.1099/ijs.0.64562-0DOI Listing
December 2006
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