Phage-host interactions in soil

Marsh, Peter; Wellington, Elizabeth M. H.

doi:10.1111/j.1574-6941.1994.tb00234.x

Cited by 101 publications

(77 citation statements)

References 41 publications

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“…Such a mechanism could also lead to reduced viral adsorption coefficients in prokaryotic virus-host systems. In addition, it has been argued that inhibitors such as endolysins released during lysis may sweep receptors on prokaryotes (Marsh and Wellington 1994), also resulting in reduced viral adsorption coefficients. As inhibitors are probably released concomitantly with viruses, such mechanisms should be strongest in summer when viral abundance and viral infection rates were high.…”

Section: Discussionmentioning

confidence: 99%

Linking bacterial richness with viral abundance and prokaryotic activity

Winter

Smit

Herndl

et al. 2005

Limnology & Oceanography

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We measured relative bacterial and archaeal richness and its covariation with physical and other biological parameters during six cruises in the North Sea over prokaryotic productivity levels ranging over two orders of magnitude. Relative bacterial and archaeal richness was estimated as the number of peaks detected by terminalrestriction fragment length polymorphism (T-RFLP) analysis of polymerase chain reaction-amplified prokaryotic 16S rRNA gene fragments in unfiltered (total community) and 0.8-m filtered seawater (free-living community). Relative bacterial richness ranged from 20 to 57 peaks in the total community and from 16 to 56 peaks in the freeliving community. Relative archaeal richness varied between 2 and 14 peaks in the total community and between 2 and 21 peaks in the free-living community. Coamplified plastid DNA might have influenced relative bacterial richness in unfiltered but not in 0.8-m filtered seawater. Relative bacterial richness decreased with viral abundance and total and cell-specific prokaryotic production in the free-living and the total community. Stepwise multiple regression analysis revealed that temperature also influenced relative bacterial richness. Relative archaeal richness was not related to any other parameter. The data suggest that high prokaryotic productivity was sustained by a relatively small number of highly active bacterial populations that also maintained high viral abundance.The advent of molecular techniques prompted the discovery of highly diverse prokaryotic communities in aquatic environments. As a consequence, the question arose how such high prokaryotic diversity can be maintained in relatively homogenous aquatic environments with only a limited number of resources. This problem was first noted for phytoplankton and later extended to bacterioplankton. However, it also has been argued that the high complexity of dissolved organic matter and the large number of different metabolic pathways of prokaryotes allow for a large number of niches and, thus, offer the possibility of an alternative theory where high prokaryotic diversity is maintained by substrate diversity (Thingstad 2000). Three major factors are thought to regulate the composition of bacterioplankton: the availability of resources, size-selective grazing on prokaryotes mainly by heterotrophic nanoflagellates, and viral lysis. The influence of protozoan grazing and the availability of resources on the composition of prokaryotic communities have been demonstrated by a number of studies (e.g., Š imek et al. 2003). Also, prokaryotic communities can be affected by AcknowledgmentsWe thank the captain and the crew of R/V Pelagia for their support at sea. We thank Martien Baars and Corina Brussaard for their efforts as cruise leaders and the opportunity to join their cruises and Maite Pérez, Ingrid Obernosterer, and Thomas Reinthaler for contributing to the prokaryotic production measurements. Frede Thingstad kindly provided suggestions on a draft of the manuscript. Two anonymous reviewers provided v...

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Section: Discussionmentioning

confidence: 99%

Linking bacterial richness with viral abundance and prokaryotic activity

Winter

Smit

Herndl

et al. 2005

Limnology & Oceanography

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“…While it makes evolutionary sense that lysogeny is an adaptation to low host abundance, an explanation is required for the finding of low FLC values at high bacterial abundance, since there is no a priori reason why lysogeny should be disadvantageous in such conditions. The number of genomes of a prophage population depends on the replication rate of the host resulting in one additional viral genome per cell division (Marsh and Wellington 1994), whereas lysis results in multiple genome copies determined by the burst size. At the community level, prophage replication rate was only two times higher in surface waters than in mesopelagic and deep waters, whereas viral production was about two orders of magnitude higher (Table 1).…”

Section: Relationship Between Lysogeny and Lytic Viral Infection-mentioning

confidence: 99%

“…Viral lysis might also influence species diversity by ''killing the winner'' (Thingstad and Lignell 1997) and keeping in check competitive dominants . Lysogeny confers some immunity against infection by related phages, and prophages can also change the metabolic properties of hosts and by that the fitness of lysogens (Marsh and Wellington 1994). This may result in virus-induced changes of species diversity as well.…”

mentioning

confidence: 99%

Lysogeny and virus‐induced mortality of bacterioplankton in surface, deep, and anoxic marine waters

Weinbauer

Brettar

Höfle

2003

Limnology & Oceanography

285

299

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Lysogeny (bacteria containing inducible prophages) and lytic viral infection (bacteria in a lytic stage of infection) were investigated at the community level in contrasting marine environments such as estuarine versus offshore waters, surface versus deep waters, and oxic versus anoxic waters in the Mediterranean and Baltic Seas. The frequency of lysogenic cells (FLC) in bacterioplankton communities ranged from not detectable to 84% as estimated by prophage induction due to mitomycin C, and highest values were typically found in deep waters (800-2,000 m). Transmission electron microscopy based estimates of virus-induced mortality of bacterioplankton (VMB) ranged from a few percent to 71%, and highest values were found in anoxic waters of the Baltic Sea. FLC and the frequency of infected cells (FIC) were related in form of a negative power function indicating that environments exist where one of the two viral life strategies prevails. Across all investigated environments, FLC was negatively related to bacterial abundance and production, whereas FIC showed a positive relationship with viral and bacterial parameters. FIC was higher and FLC was lower in moderately productive estuarine and offshore surface waters than in less productive mesopelagic and deep waters. Thus, lysogeny seems to be a survival strategy at low host abundance and activity, whereas high host abundance and activity seems to favor the lytic life cycle. The key process for the prevalence of lytic infection compared to prophage replication at high host abundance could be competition due to outnumbering. Between 11% and 88% (average, 35%) of the bacteria contained a functional (lytic or lysogenic) viral genome.Viruses play a significant role in ecological and biogeochemical processes of the ocean, and their impact depends on the reproductive pathway (Fuhrman 1999; Wilhelm and Suttle 1999; Wommack and Colwell 2000). The two major viral reproductive strategies are lysogeny and lytic viral infection. In the lytic cycle, the (bacterio)phage forces the host metabolism to produce new phages, which are released during the lysis of the cell. In the lysogenic cycle, the lysogenic phage either enters the lytic cycle directly or the phage genome remains within the host in a dormant stage (prophage) and replicates along with the host until the lytic cycle is induced. In the pseudolysogenic life cycle, a fraction of the infected population is lysed (Ackermann and DuBow 1987); however, this has not been studied at the community level.Based on studies with isolated phage-host systems and using models, it was proposed that lysogeny is a survival strategy of phages at low host densities (Steward and Levin 1984). Consequently, reproduction of lytic phages should be 1 To whom correspondence should be addressed. Present address: Laboratoire d'Océanographie de Villefranche-sur-Mer (LOV), UMR 7093 CNRS-UPMC, BP 28, 06234 Villefranche-sur-Mer (wein@ obs-vlfr.fr). AcknowledgmentsThe captains and the crews of R/V Thetys II and the R/V Aranda are gratefully acknowled...

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“…Lysogeny is characterized by two distinct phases that could influence the BCC with contrasting outcomes. The establishment of lysogeny confers immunity against infection by the same or closely related phages, and prophages can also change the growth properties of their host (Levin and Lenski, 1983;Marsh and Wellington, 1994), generally leading to the increase in their abundance (Edlin et al, 1975;Paul, 2008). Here, we propose that these benefits of lysogeny also exist within natural bacterioplankton, probably conferring a selective advantage to some groups that will eventually become abundant in the community.…”

Section: Changes In Bcc Upon Induction and Ecological Considerationsmentioning

confidence: 83%

Disentangling the relative influence of bacterioplankton phylogeny and metabolism on lysogeny in reservoirs and lagoons

et al. 2010

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Previous studies indicate that lysogeny is preponderant when environmental conditions are challenging for the bacterial communities and when their metabolism is reduced. Furthermore, it appears that lysogeny is more frequent within certain bacterial phylogenetic groups. In this comparative study from 10 freshwater reservoirs and 10 coastal lagoons, we aim to disentangle the influence of these different factors. In eight reservoirs and four lagoons, lysogeny was detected by induction assays with mitomycin C, and induction significantly modified the bacterial community composition (BCC), whereas community composition remained constant in ecosystems in which lysogeny was not observed. Among the phylogenetic groups studied, the most abundant ones were Bacteroidetes and a-proteobacteria in lagoons, and b-proteobacteria and Bacteroidetes in reservoirs. These dominant groups comprised the highest proportions of inducible lysogens. In order to unravel the effects of bacterial metabolism from phylogeny on lysogeny, we measured bacterial community physiology and the specific activities of selected phylogenetic groups. The proportion of inducible lysogens within the a-and the b-proteobacteria decreased with increasing group-specific metabolism in lagoons and reservoirs, respectively. In contrast, this relationship was not observed for the other lysogen-containing groups. Hence, both host physiology and phylogeny are critical for the establishment of lysogeny. This study illustrates the importance of lysogeny among the most abundant phylogenetic groups, and further suggests its strong structuring impact on BCC.

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Phage-host interactions in soil

Cited by 101 publications

References 41 publications

Linking bacterial richness with viral abundance and prokaryotic activity

Linking bacterial richness with viral abundance and prokaryotic activity

Lysogeny and virus‐induced mortality of bacterioplankton in surface, deep, and anoxic marine waters

Disentangling the relative influence of bacterioplankton phylogeny and metabolism on lysogeny in reservoirs and lagoons

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