Marine Phages As Tracers: Effects of Size, Morphology, and Physico–Chemical Surface Properties on Transport in a Porous Medium

Ghanem, Nawras; Kiesel, Bärbel; Kallies, René; Harms, Hauke; Chatzinotas, Antonis; Wick, Lukas Y.

doi:10.1021/acs.est.6b04236

Cited by 23 publications

(56 citation statements)

References 85 publications

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“…Phage T4, for example, is similarly unable to infect stationary phase E. coli cells, but phage T7 can (33, 56). Other phages of different sizes or hydrophobicities may be better or worse at diffusing through biofilm (57). Second, it is possible that a greater protective effect between our particular strains would be observed under different growth conditions, for example if we were to provide our bacteria with nutrients that were constantly replenished to limit growth arrest.…”

Section: Discussionmentioning

confidence: 99%

Phage efficacy in infecting dual-strain biofilms ofPseudomonas aeruginosa

Testa

Berger

Piccardi

et al. 2019

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Bacterial viruses, or phage, play a key role in shaping natural 1 microbial communities. Yet much research on bacterial-phage 2 interactions has been conducted in liquid cultures involving sin-3 gle bacterial strains. Critically, phage often have a very narrow 4 host range meaning they can only ever target a subset of strains 5 in a community. Here we explore how strain diversity affects 6 the success of lytic phage in structured communities. In par-7 ticular, we infect a susceptible Pseudomonas aeruginosa strain 8 PAO1 with lytic phage Pseudomonas 352 in the presence versus 9 absence of an insensitive P. aeruginosa strain PA14, in liquid cul-10 ture versus colonies growing on agar. We find that competition 11 between the two bacterial strains reduces the likelihood of the 12 susceptible strain evolving resistance to the phage. This result 13 holds in liquid culture and in colonies. However, while in liq-14 uid the phage eliminate the whole sensitive population, colonies 15 contain refuges wherein bacteria can remain sensitive yet es-16 cape phage infection. These refuges form mainly due to reduced 17 growth in colony centers. We find little evidence that the pres-18 ence of the insensitive strain provides any additional protection 19 against phage. Our study reveals that living in a spatially struc-20 tured population can protect bacteria against phage infection, 21 while the presence of competing strains may instead reduce the 22 likelihood of evolving resistance to phage, if encountered. 23 Bacterial colony | resistance | evolution | microbial communities | population 24 dynamics | spatial structure | phage therapy 25 Correspondence: sara.mitri@unil.ch 26 82 survival rate compared to planktonic bacteria (25), particu-83 larly when exposed to antibiotics and importantly, also to 84 phage (26). More generally, phage population dynamics dif-85 fer radically between liquid bacterial cultures and bacteria 86 growing on solid surfaces (27). 87 Here we show that both of these factors -the presence of 88 other strains, and spatial structure -separately and combined 89 affect the outcome of phage predation on the pathogen Pseu-90 Testa et al. | bioRχiv | February 15, 2019 | 1-10In particular, we target P. aeruginosa strain PAO1 with Pseu-92 domonas phage 352 to which it is sensitive, in the presence 93 and absence of a second strain, P. aeruginosa PA14 that is in-94 sensitive to the phage. Since phage are so specific, we believe 95 the choice of a closely-related phage-insensitive strain to be 96 a realistic one. We compare the outcome for PAO1 in a well-97 mixed liquid environment and a structured biofilm (colony) 98 growing on a solid agar surface. 99 We find that in liquid, competition between the two strains 100 can reduce the population size of the target strain PAO1, giv-101 ing a competitive advantage to the phage and eliminating 102 PAO1 without the emergence of resistance. Indeed, evolv-103 ing resistance to the phage was the only way for PAO1 to 104 survive phage attack in liquid. In contrast, in a biofilm...

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Section: Discussionmentioning

confidence: 99%

Phage efficacy in infecting dual-strain biofilms ofPseudomonas aeruginosa

Testa

Berger

Piccardi

et al. 2019

Preprint

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“…Rainfall could have two main effects for soil viral communities: (i) Intense rainfall may lead to virus removal by flushing viruses out of the soil as discussed above. As different viruses have different physical properties such as surface charge or hydrophobicity, they are also flushed out at different rates (Ghanem et al, 2016 ). (ii) An intermediate amount of rainfall leads to increased soil moisture, can enhance the microbial activity and influence the bacterial community composition (Zhang et al, 2013 ), which then probably affects also the viral production and community composition.…”

Section: Discussionmentioning

confidence: 99%

Soil Viral Communities Vary Temporally and along a Land Use Transect as Revealed by Virus-Like Particle Counting and a Modified Community Fingerprinting Approach (fRAPD)

et al. 2017

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Environmental surveys on soil viruses are still rare and mostly anecdotal, i. e., they mostly report on viruses at one location or for only a few sampling dates. Detailed time-series analysis with multiple samples can reveal the spatio-temporal dynamics of viral communities and provide important input as to how viruses interact with their potential hosts and the environment. Such surveys, however, require fast, easy-to-apply and reliable methods. In the present study we surveyed monthly across 13 months the abundance of virus-like particles (VLP) and the structure of the viral communities in soils along a land use transect (i.e., forest, pasture, and cropland). We evaluated 32 procedures to extract VLP from soil using different buffers and mechanical methods. The most efficient extraction was achieved with 1× saline magnesium buffer in combination with 20 min vortexing. For community structure analysis we developed an optimized fingerprinting approach (fluorescent RAPD-PCR; fRAPD) by combining RAPD-PCR with fluorescently labeled primers in order to size the obtained fragments on a capillary sequencing machine. With the concomitantly collected data of soil specific factors and weather data, we were able to find correlations of viral abundance and community structure with environmental variables and sampling site. More specifically, we found that soil specific factors such as pH and total nitrogen content played a significant role in shaping both soil viral abundance and community structure. The fRAPD analysis revealed high temporal changes and clustered the viral communities according to sampling sites. In particular we observed that temperature and rainfall shaped soil viral communities in non-forest sites. In summary our findings suggest that sampling site was a key factor for shaping the abundance and community structure of soil viruses, and when site vegetation was reduced, temperature and rainfall were also important factors.

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“…In muddy and subsurface sediments, import and export of viruses are restricted to diffusion, whereas in sandy sediments both processes might contribute significantly to virus numbers as advection accelerates porewater transport and exchange between porewater and bottom water (Ahmerkamp, 2016 ). However, many viruses adsorb to the sediment matrix after production and during transport (Dowd et al, 1998 ; Ghanem et al, 2016 ).…”

Section: Discussionmentioning

confidence: 99%

“…For the experiments with flow-through reactors, virus numbers in the effluents unlikely represented the gross virus production inside the sediment columns. Instead, viruses partly absorbed to sediment grains depending on the physicochemical surface properties of the respective virus, which includes size, hydrophobicity and morphology of the virus (Ghanem et al, 2016 ). Moreover, sorption of viruses is also dependent on the pH of the solution, redox conditions and organic matter content of sediments (Klitzke et al, 2015 ).…”

Section: Discussionmentioning

confidence: 99%

“…Due to their small size, viruses can be transported by advective flow through permeable sands. The transport of viruses can be halted by sorption to sediment grains which has been shown to depend strongly on size and surface characteristic of the respective virus but also on the water composition and surface characteristics of the sand (Bales et al, 1995 ; Dowd et al, 1998 ; Ghanem et al, 2016 ). Virus numbers in marine sediments range from 10 3 to 10 10 viruses cm −3 (Carreira et al, 2013 ; Engelhardt et al, 2014 ; Yanagawa et al, 2014 ).…”

Section: Introductionmentioning

confidence: 99%

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Virus Dynamics Are Influenced by Season, Tides and Advective Transport in Intertidal, Permeable Sediments

2017

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Sandy surface sediments of tidal flats exhibit high microbial activity due to the fast and deep-reaching transport of oxygen and nutrients by porewater advection. On the other hand during low tide, limited transport results in nutrient and oxygen depletion concomitant to the accumulation of microbial metabolites. This study represents the first attempt to use flow-through reactors to investigate virus production, virus transport and the impact of tides and season in permeable sediments. The reactors were filled with intertidal sands of two sites (North beach site and backbarrier sand flat of Spiekeroog island in the German Wadden Sea) to best simulate advective porewater transport through the sediments. Virus and cell release along with oxygen consumption were measured in the effluents of reactors during continuous flow of water through the sediments as well as in tidal simulation experiments where alternating cycles with and without water flow (each for 6 h) were operated. The results showed net rates of virus production (0.3–13.2 × 106 viruses cm−3 h−1) and prokaryotic cell production (0.3–10.0 × 105 cells cm−3 h−1) as well as oxygen consumption rates (56–737 μmol l−1 h−1) to be linearly correlated reflecting differences in activity, season and location of the sediments. Calculations show that total virus turnover was fast with 2 to 4 days, whereas virus-mediated cell turnover was calculated to range between 5–13 or 33–91 days depending on the assumed burst sizes (number of viruses released upon cell lysis) of 14 or 100 viruses, respectively. During the experiments, the homogenized sediments in the reactors became vertically structured with decreasing microbial activities and increasing impact of viruses on prokaryotic mortality with depth. Tidal simulation clearly showed a strong accumulation of viruses and cells in the top sections of the reactors when the flow was halted indicating a consistently high virus production during low tide. In conclusion, cell lysis products due to virus production may fuel microbial communities in the absence of advection-driven nutrient input, but are eventually washed off the surface sediment during high tide and being transported into deeper sediment layers or into the water column together with the produced viruses.

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Marine Phages As Tracers: Effects of Size, Morphology, and Physico–Chemical Surface Properties on Transport in a Porous Medium

Cited by 23 publications

References 85 publications

Phage efficacy in infecting dual-strain biofilms ofPseudomonas aeruginosa

Phage efficacy in infecting dual-strain biofilms ofPseudomonas aeruginosa

Soil Viral Communities Vary Temporally and along a Land Use Transect as Revealed by Virus-Like Particle Counting and a Modified Community Fingerprinting Approach (fRAPD)

Virus Dynamics Are Influenced by Season, Tides and Advective Transport in Intertidal, Permeable Sediments

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