Dissecting the role of viruses in marine nutrient cycling: bacterial uptake of D- and L-amino acids released by viral lysis

Shelford, Emma J.; Jørgensen, Niels O. G.; Rasmussen, Susan B.; Suttle, Curtis A.; Middelboe, Mathias

doi:10.3354/ame01720

Cited by 4 publications

(5 citation statements)

References 67 publications

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“…The same could be said for the nutrients, except for particulate phosphorus, for which significant changes occurred with a significant increase and decrease in the VA+ and VA/VA− treatments, respectively. It was, however, difficult to establish a clear association between the viral and nutrient dynamics, while recent studies have demonstrated the importance of the viruses in producing dissolved organic matter or inorganic nutrients through cell lysis and their use by non-infected populations ( Shelford et al, 2012 , 2014 ).…”

Section: Discussionmentioning

confidence: 99%

“…Finally, Dean et al (2008) revealed that bacterial lysis by viruses in Lake Erie could release fairly large quantities of phosphorus each day, suggesting a major role in the recycling of phosphorus. Currently, there is no longer any doubt that the virus-induced influx of organic matter can enhance bacterial production and fuels the microbial loop and the cycling of inorganic nutrients (see Shelford et al, 2014 and references therein).…”

Section: Introductionmentioning

confidence: 99%

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Do phages impact microbial dynamics, prokaryotic community structure and nutrient dynamics in Lake Bourget?

Meunier¹,

Jacquet²

2015

Biology Open

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Phages are the most abundant and diversified biological entities in aquatic ecosystems. Understanding their functional role requires laboratory experiments on a short time-scale. Using samples of surface waters of Lake Bourget, we studied whether viruses impact (i) the abundance patterns of the bacterial and phytoplankton communities, (ii) a part of the prokaryotic community composition (both for Eubacteria and Archaea), and (iii) the recycling of nutrients and/or organic matter. Three experiments were performed (one each in February, March and April) at the transition between winter and spring in 2013. The experiment reduced or increased the abundance of virus-like particles in samples containing only the picoplanktonic fraction. Viral and cellular abundances, bacterial and archaeal community structures as well as nutrient concentrations were analysed every 24 h for 3 days. Some of the results reveal that increasing the phage abundance increased the diversity of the eubacterial community. Consistent with the ‘killing the winner’ concept, viruses are thus likely to significantly change the composition of the bacterial community. This suggests a positive association between viral abundance and bacterial diversity. In contrast, the composition of the archaeal community did not seem to be affected by phage abundance, suggesting the absence of viral control on this community or the inability to observe it at this period of year, either based on the time scale of the investigation or because the archaeal virus titre was too low to induce a significant and visible effect. Lastly, we were unable to demonstrate viruses driving the cycling of nutrients or the response of plankton to nutrient concentration changes in a significant way, suggesting that the role of viruses may be subtle or difficult to assess through the use of such experimental procedures.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Do phages impact microbial dynamics, prokaryotic community structure and nutrient dynamics in Lake Bourget?

Meunier¹,

Jacquet²

2015

Biology Open

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“…The net effect of the so‐called ‘viral loop’ is that it ultimately converts organic matter into dissolved inorganic nutrients, including respired CO 2 (Wilhelm & Suttle, ; Haaber & Middelboe, ; Pollard & Ducklow, ). Studies with marine microorganisms have revealed that viruses can be key players in nitrogen cycling (Haaber & Middelboe, ; Shelford et al ., ). In culture experiments, phage infection alters both host metabolism and lysate composition (Weinbauer & Peduzzi, ; Ankrah et al ., ; Sheik et al ., ).…”

Section: Viral Impact On Water Biochemistry and Carbon Flowmentioning

confidence: 97%

“…In the river‐influenced False Creek (Vancouver, Canada), experiments demonstrated that viral lysis leads to ammonium production from liberation of dissolved organic N that is re‐mineralised by uninfected bacteria, thus fuelling primary production (Shelford et al ., ). Nonetheless, a net uptake of ammonium by non‐infected bacteria in other culture experiments revealed that the metabolism of viral lysates can also result in net consumption of inorganic N (Shelford et al ., ). This recent evidence suggests that viral lysis of microbes changes the relative distribution of dissolved organic (and also inorganic) matter with many indirect effects on the aquatic systems (Weitz & Wilhelm, ).…”

Section: Viral Impact On Water Biochemistry and Carbon Flowmentioning

confidence: 97%

Virus ecology of fluvial systems: a blank spot on the map?

Peduzzi

2015

Biological Reviews

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The ecology of viruses has been studied only in a limited number of rivers and streams. In light of a recent re‐appraisal of the global fluvial surface area, issues such as abundance and production, host mortality and the influence of suspended particles and biofilms are addressed. Viral life cycles, potential impacts of viruses on water biochemistry and carbon flow, and viral diversity are considered. Variability in trophic levels along with the heterogeneous nature and hydrological dynamics of fluvial environments suggest a prevailingly physical control of virus‐related processes under lotic conditions and more biological control under lentic conditions. Viral lysis likely contributes to a pool of rapidly cycling carbon in environments typically characterized by high proportions of recalcitrant terrestrial carbon. On average, 33.6% (equalling 0.605 Pg C year−1) of the globally respired carbon from fluvial systems may pass through a viral loop. Virus distribution and the proportion of organic material in horizontal transport versus processes in retention zones remain to be determined in detail. The need for up‐scaling the contribution of virus‐related processes in fluvial systems is of global relevance. Further, the role of climate change and the effect of anthropogenic alterations of fluvial systems on viruses require attention. The identification of these considerable knowledge gaps should foster future research efforts.

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“…The microbial utilization of D -amino acids has been studied mainly in soils and is regarded as common in soil microorganisms (e.g., Hill et al, 2011 ; Broughton et al, 2015 ; Radkov et al, 2016 ). D -amino acid utilization by marine microbiota has also been studied (e.g., Perez et al, 2003 ; Azúa et al, 2014 ; Shelford et al, 2014 ); however, only a few D -amino acid utilizers have been isolated. As a deep-sea strain, Phaeobacter sp.…”

Section: Introductionmentioning

confidence: 99%

Enhanced Bacterial Growth and Gene Expression of D-Amino Acid Dehydrogenase With D-Glutamate as the Sole Carbon Source

et al. 2018

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In a search for life-supporting, not life-assisting, D-amino acid metabolism, an environmental strain that grows better with D-glutamate as the sole carbon source was isolated from an ordinary river. The strain, designated as A25, exhibited a faster growth rate and greater cell yield with D-glutamate than with L-glutamate. Conversely, the D/L ratio of total cellular glutamate was as low as 4/96, which suggests that D-glutamate is more likely catabolized than anabolized. Strain A25 was phylogenetically most closely related to the gamma-proteobacterial species Raoultella ornithinolytica, with a 16S rRNA gene sequence similarity of 100%. A standard strain, R. ornithinolytica JCM 6096T, also showed similarly enhanced growth with D-glutamate, which was proven for the first time. Gene expression of the enzymes involved in D-amino acid metabolism was assayed by reverse-transcription quantitative PCR (RT-qPCR) using specifically designed primers. The targets were the genes encoding D-amino acid dehydrogenase (DAD; EC 1.4.99.1), glutamate racemase (EC 5.1.1.3), D-glutamate oxidase (EC 1.4.3.7 or EC 1.4.3.15), and UDP-N-acetyl-α-D-muramoyl-L-alanyl-D-glutamate ligase (EC 6.3.2.9). As a result, the growth of strains A25 and R. ornithinolytica JCM 6096T on D-glutamate was conspicuously associated with the enhanced expression of the DAD gene (dadA) in the exponential phase compared with the other enzyme genes. Pseudomonas aeruginosa is also known to grow on D-glutamate as the sole carbon source but to a lesser degree than with L-glutamate. A standard strain of P. aeruginosa, JCM 5962T, was tested for gene expression of the relevant enzymes by RT-qPCR and also showed enhanced dadA expression, but in the stationary phase. Reduction of ferricyanide with D-glutamate was detected in cell extracts of the tested strains, implying probable involvement of DAD in the D-glutamate catabolizing activity. DAD-mediated catalysis may have advantages in the one-step production of α-keto acids and non-production of H2O2 over other enzymes such as racemase and D-amino acid oxidase. The physiological and biochemical importance of DAD in D-amino acid metabolism is discussed.

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Dissecting the role of viruses in marine nutrient cycling: bacterial uptake of D- and L-amino acids released by viral lysis

Cited by 4 publications

References 67 publications

Do phages impact microbial dynamics, prokaryotic community structure and nutrient dynamics in Lake Bourget?

Do phages impact microbial dynamics, prokaryotic community structure and nutrient dynamics in Lake Bourget?

Virus ecology of fluvial systems: a blank spot on the map?

Enhanced Bacterial Growth and Gene Expression of D-Amino Acid Dehydrogenase With D-Glutamate as the Sole Carbon Source

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