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Differentiation of Rhizobium and phage communities. A and B PCoA plots illustrating the differences in chromosomal composition between Rhizobium communities across common bean populations based on Jaccard distances (presence-absence) and Bray-Curtis distances (relative abundance), respectively. D and E PCoA plots showing the differences in the phage genomic type composition between phage communities across common bean populations based
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Bacteriophages play significant roles in the composition, diversity, and evolution of bacterial communities. Despite their importance, it remains unclear how phage diversity and phage-host interactions are spatially structured. Local adaptation may play a key role. Nitrogen-fixing symbiotic bacteria, known as rhizobia, have been shown to locally ad...
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... first aim was to investigate whether the collected Rhizobium strains represent geographically structured populations. Phylogenetic analysis of the partial recA-dnaB sequences of 229 rhizobial strains identified R. etli as the predominant species at Mexican sampling sites (74.6%), while R. phaseoli was dominant in Argentina (80%) ( Fig. 1; Fig. S2a). According to the nucleotide variations in recA and dnaB, all of the isolated rhizobia were grouped into 41 chromosomal STs (Table S4). PERMANOVA tests employing two distance measures (Jaccard and Bray-Curtis) indicated that the rhizobial communities differed significantly in terms of genetic composition and the relative abundance of ...
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... and dnaB, all of the isolated rhizobia were grouped into 41 chromosomal STs (Table S4). PERMANOVA tests employing two distance measures (Jaccard and Bray-Curtis) indicated that the rhizobial communities differed significantly in terms of genetic composition and the relative abundance of genotypes (STs) among different bean fields and regions ( Fig. 2A-C; Table S4-S5). The geographic distance between the regions, represented by a PCNM vector, was correlated with the ST composition among the rhizobia isolated from the four common bean fields (Table S5). At the species level, R. etli and R. phaseoli STs differed significantly among the sites of origin of the common bean fields. Between ...
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... of the common bean fields. Between regions, only the R. etli populations differed in terms of the ST composition, whereas the R. phaseoli ST composition changed only marginally across regions (Table S5). The abundance of ST-5 in R. phaseoli, the only ST of the 41 total STs found across the four common bean fields, might explain this last result ( Fig. 2C; Table ...
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... phage families were present at the four sampling sites, but the Salta community was dominated by Myoviridae (69%) and the Chicoana community by Siphoviridae (62%) ( Fig. S2b; Table S7). The Microviridae family (F02), defined by small-genome phages (4.8-6.2 kb), was dominant in Tepoztlán (60%), whereas it showed low abundance or was absent in the other populations (0-23%; Table ...
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... the differences in the rhizobial ST composition per sampling site, we found that the composition of PGTs also differed significantly among common bean fields and regions (Fig. 2 D-F, Table S7). The differences were significantly correlated with geographic distance (Table S5). The phage communities were also significantly different between the Mexican bean fields within regions based on Jaccard distances (F 1,5 = 3.7, p = 0.024), but they were not significantly different between Mexican bean fields based on ...
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... 1,5 = 2.2, p = 0.149). Mantel tests showed that the genetic composition differences among phage communities were significantly correlated with the differences in the Rhizobium community genetic composition among bean fields (Table S5). Some PGTs coexisted at two of the sampling sites, whereas PGTs rarely coexisted at three sites and never at four (Fig. 2F). Moreover, 52% of the 29 PGTs occurred solely in one bean field, and 69% were restricted to a particular region. A spatial pattern distinction was also shown by the ANI values, as the average ANI of allopatric phages belonging to the same PGTs was 88%. In comparison, the average ANI of sympatric phages belonging to the same PGT was ...
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... RPGs were singletons, whereas 19 were formed by more than two strains (maximum of 40) (Table S3). Thirty-two RPGs belonged to R. etli, twelve RPGs corresponded to R. phaseoli (RPG 4, 13, 19, 20, 22, 23, 24, 27, 31, 32, 33 & 37), and the other four RPGs belonged to both species (RPG 1, 2, 6, and 11) most abundant RPGs (1-4) were composed of the frequently identified STs of R. phaseoli (ST-5) and R. etli (ST10 and ST34). We found that the RPG composition was strongly correlated with the ST composition (Table S8). ...
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... Since the proposed re-classification of microviruses by Kirchberger et al. 19 has not been approved by ICTV yet, we tentatively classified these six roseophages into the subfamily Occultatumvirinae. Occultatumvirinae phages were firstly isolated on Rhizobium, and Rhizobium microviruses were grouped into two clusters, chaparroviruses and chicoviruses 30,31 . To the best of our knowledge, this is the first isolation of marine Occultatumvirinae phages. ...
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... Among negative interactions, predation by protozoa or bacteria (Bdellovibrio or Myxococcus) can alter rhizobial populations (Danso et al., 1975;Keya and Alexander, 1975;Ramirez and Alexander, 1980). Soil bacteriophages, which have been shown to rapidly adapt to local bacterial host communities, can also reduce the rhizobial density in the rhizosphere (Van Cauwenberghe et al., 2021). Finally, the presence of antimicrobial compounds produced by other rhizosphere microorganisms such as antibiotics produced by Actinomycetes is likely to inhibit the growth of rhizobia (Patel, 1974;Pugashetti et al., 1982). ...
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... phages, predators, and antibiotics). In particular, phages are likely to play an important role in mediating within-species apparent competition ( Figure 1b) given that the phage host range is strain-specific, and there is evidence of the coevolution of rhizobia and phage populations in natural environments [11]. Similarly, many rhizobia encode bacteriocins (narrow-range antimicrobial protein toxins) that can directly alter competition between strains in, for instance, peat media [12]. ...
Rhizobial bacteria have complex lifestyles that involve growth and survival in bulk soil, plant rhizospheres and rhizoplanes, legume infection threads, and mature and senescing legume nodules. In nature, rhizobia coexist and compete with many other rhizobial strains and species to form host associations. We review recent work defining competitive interactions across these environments. We highlight the use of sophisticated measurement tools and sequencing technologies to examine competition mechanisms in planta, and highlight environments (e.g. soil and senescing nodules) where we still know exceedingly little. We argue that moving toward an explicitly ecological framework (types of competition, resources, and genetic differentiation) will clarify the evolutionary ecology of these foundational organisms and open doors for engineering sustainable, beneficial associations with hosts.
... At the same time, coevolution can also improve the rate of phage's evolution [164]. However, the role of the community environment in the interaction between bacteria and phages is not fully understood, and many problems still need to be further explored [165]. ...
Bacteria have developed different mechanisms to defend against phages, such as preventing phages from being adsorbed on the surface of host bacteria; through the superinfection exclusion (Sie) block of phage’s nucleic acid injection; by restricting modification (R-M) systems, CRISPR-Cas, aborting infection (Abi) and other defense systems to interfere with the replication of phage genes in the host; through the quorum sensing (QS) enhancement of phage’s resistant effect. At the same time, phages have also evolved a variety of counter-defense strategies, such as degrading extracellular polymeric substances (EPS) that mask receptors or recognize new receptors, thereby regaining the ability to adsorb host cells; modifying its own genes to prevent the R-M systems from recognizing phage genes or evolving proteins that can inhibit the R-M complex; through the gene mutation itself, building nucleus-like compartments or evolving anti-CRISPR (Acr) proteins to resist CRISPR-Cas systems; and by producing antirepressors or blocking the combination of autoinducers (AIs) and its receptors to suppress the QS. The arms race between bacteria and phages is conducive to the coevolution between bacteria and phages. This review details bacterial anti-phage strategies and anti-defense strategies of phages and will provide basic theoretical support for phage therapy while deeply understanding the interaction mechanism between bacteria and phages.
... With our results, these earlier works support the conclusion that broader host ranges are not being selected for but if sufficient phages are isolated, some of these will have broader host ranges by chance. This is consistent with the observation that bacteriophages in natural systems may be specialists (narrow host range) whereas others may be generalists (broader host range) in terms of the hosts they can reproduce on [26,27]. * Unless otherwise indicated, all the host range testing strains (column 4) were strains of the phage target species (column 1). ...
Bacteriophage host range is a result of the interactions between phages and their hosts. For phage therapy, phages with a broader host range are desired so that a phage can infect and kill the broadest range of pathogen strains or related species possible. A common, but not well-tested, belief is that using multiple hosts during the phage isolation will make the isolation of broader host range phage more likely. Using a Bacillus cereus group system, we compared the host ranges of phages isolated on one or four hosts and found that there was no difference in the breadth of host ranges of the isolated phages. Both narrow and broader host range phage were also equally likely to be isolated from either isolation procedure. While there are methods that reliably isolate broader host range phages, such as sequential host isolation, and there are other reasons to use multiple hosts during isolation, multiple hosts are not a consistent way to obtain broader host range phages.
... Так, в экспериментах по перекрёстному инфицированию фаги азотфиксирующих бактерий Rhizobium spp. из Мексики и Аргентины проявляли большую активность в отношении локальных штаммов микроорганизмов [67]. Бактериофаг A.baumannii из Юго-западного госпиталя, расположенного в муниципалитете Чунцин (Китай), проявлял литическую активность в отношении всех 10 протестированных локальных изолятов (100%). ...
One of the central topics in bacteriophage research is the host specificity. It depends on the success of completing viral life cycle stages, including adsorption, penetration of the genetic material of the virus into the cell and its replication, assembly of phage particles and cell lysis. Laboratory assessments of the spectrum of lytic activity of phages are inextricably linked to significant methodological biases, and the often used spot test method can be associated with a large percentage of false-positive results. Along with the variety of types of phage specificity, there is temporal variability. The co-evolution of phages and bacteria leads to the acquisition of resistance to viruses by bacteria and the accumulation of mutations in the genomes of bacteriophages aimed at overcoming this resistance. At the same time, the adaptation of bacteriophages to bacteria that are evolutionarily distant from the isolation hosts is barely possible. This barrier is based on the peculiarities of metabolism, cell wall structures and mechanisms for the implementation of matrix processes. The spatial factor of phage specificity is manifested in the greater breadth of the spectra of lytic activity of bacteriophages on local samples of bacteria compared to the spectra assessed on samples of isolates from habitats geographically distant from the place of virus isolation.
... A study in soil microcosms demonstrated that the fitness cost of phage resistance among bacteria limited their resistance to include only co-occurring phages [104]. Meanwhile, among soil phages, a high level of local adaptation has been shown to result in greater infection rates of co-existing rhizobia strains, as compared to geographically distant strains [105]. Therefore, given the elevated fitness cost of resistance, specific to the rhizosphere [54], newly colonising bacteria are likely to be susceptible to primed viruses. ...
Background
The rhizosphere is a hotspot for microbial activity and contributes to ecosystem services including plant health and biogeochemical cycling. The activity of microbial viruses, and their influence on plant-microbe interactions in the rhizosphere, remains undetermined. Given the impact of viruses on the ecology and evolution of their host communities, determining how soil viruses influence microbiome dynamics is crucial to build a holistic understanding of rhizosphere functions.
Results
Here, we aimed to investigate the influence of crop management on the composition and activity of bulk soil, rhizosphere soil, and root viral communities. We combined viromics, metagenomics, and metatranscriptomics on soil samples collected from a 3-year crop rotation field trial of oilseed rape ( Brassica napus L.). By recovering 1059 dsDNA viral populations and 16,541 ssRNA bacteriophage populations, we expanded the number of underexplored Leviviricetes genomes by > 5 times. Through detection of viral activity in metatranscriptomes, we uncovered evidence of “Kill-the-Winner” dynamics, implicating soil bacteriophages in driving bacterial community succession. Moreover, we found the activity of viruses increased with proximity to crop roots, and identified that soil viruses may influence plant-microbe interactions through the reprogramming of bacterial host metabolism. We have provided the first evidence of crop rotation-driven impacts on soil microbial communities extending to viruses. To this aim, we present the novel principal of “viral priming,” which describes how the consecutive growth of the same crop species primes viral activity in the rhizosphere through local adaptation.
Conclusions
Overall, we reveal unprecedented spatial and temporal diversity in viral community composition and activity across root, rhizosphere soil, and bulk soil compartments. Our work demonstrates that the roles of soil viruses need greater consideration to exploit the rhizosphere microbiome for food security, food safety, and environmental sustainability.
