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Phage and bacteria support mutual diversity in a narrowing staircase of coexistence.

ABSTRACT: The competitive exclusion principle states that phage diversity M should not exceed bacterial diversity N. By analyzing the steady-state solutions of multistrain equations, we find a new constraint: the diversity N of bacteria living on the same resources is constrained to be M or M+1 in terms of the diversity of their phage predators. We quantify how the parameter space of coexistence exponentially decreases with diversity. For diversity to grow, an open or evolving ecosystem needs to climb a narrowing 'diversity staircase' by alternatingly adding new bacteria and phages. The unfolding coevolutionary arms race will typically favor high growth rate, but a phage that infects two bacterial strains differently can occasionally eliminate the fastest growing bacteria. This context-dependent fitness allows abrupt resetting of the 'Red-Queen's race' and constrains the local diversity.

SUBMITTER: Haerter JO

PROVIDER: S-EPMC4992086 | biostudies-other | 2014 Nov

REPOSITORIES: biostudies-other

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Phage and bacteria support mutual diversity in a narrowing staircase of coexistence.

Haerter Jan O JO Mitarai Namiko N Sneppen Kim K

The ISME journal 20140523 11

The competitive exclusion principle states that phage diversity M should not exceed bacterial diversity N. By analyzing the steady-state solutions of multistrain equations, we find a new constraint: the diversity N of bacteria living on the same resources is constrained to be M or M+1 in terms of the diversity of their phage predators. We quantify how the parameter space of coexistence exponentially decreases with diversity. For diversity to grow, an open or evolving ecosystem needs to climb a n ...[more]

PMID: 24858781

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Project description:Bacterial communities are often exposed to temporal variations in resource availability, which exceed bacterial generation times and thereby affect bacterial coexistence. Bacterial population dynamics are also shaped by bacteriophages, which are a main cause of bacterial mortality. Several strategies are proposed in the literature to describe infections by phages, such as "Killing the Winner", "Piggyback the loser" (PtL) or "Piggyback the Winner" (PtW). The two temperate phage strategies PtL and PtW are defined by a change from lytic to lysogenic infection when the host density changes, from high to low or from low to high, respectively. To date, the occurrence of different phage strategies and their response to environmental variability is poorly understood. In our study, we developed a microbial trophic network model using ordinary differential equations (ODEs) and performed 'in silico' experiments. To model the switch from the lysogenic to the lytic cycle, we modified the lysis rate of infected bacteria and their growth was turned on or off using a density-dependent switching point. We addressed whether and how the different phage strategies facilitate bacteria coexistence competing for limiting resources. We also studied the impact of a fluctuating resource inflow to evaluate the response of the different phage strategies to environmental variability. Our results show that the viral shunt (i.e. nutrient release after bacterial lysis) leads to an enrichment of the system. This enrichment enables bacterial coexistence at lower resource concentrations. We were able to show that an established, purely lytic model leads to stable bacterial coexistence despite fluctuating resources. Both temperate phage models differ in their coexistence patterns. The model of PtW yields stable bacterial coexistence at a limited range of resource supply and is most sensitive to resource fluctuations. Interestingly, the purely lytic phage strategy and PtW both result in stable bacteria coexistence at oligotrophic conditions. The PtL model facilitates stable bacterial coexistence over a large range of stable and fluctuating resource inflow. An increase in bacterial growth rate results in a higher resilience to resource variability for the PtL and the lytic infection model. We propose that both temperate phage strategies represent different mechanisms of phages coping with environmental variability. Our study demonstrates how phage strategies can maintain bacterial coexistence in constant and fluctuating environments.

Project description:Emerging evidence supports that the phage-prokaryote interaction drives ecological processes in various environments with different phage life strategies. However, the knowledge of phage-prokaryote interaction in the shrimp culture pond ecosystem (SCPE) is still limited. Here, the viral and prokaryotic community profiles at four culture stages in the intestine of Litopenaeus vannamei and cultural sediment microhabitats of SCPE were explored to elucidate the contribution of phage-prokaryote interaction in modulating microbial communities. The results demonstrated that the most abundant viral families in the shrimp intestine and sediment were Microviridae, Circoviridae, Inoviridae, Siphoviridae, Podoviridae, Myoviridae, Parvoviridae, Herelleviridae, Mimiviridae, and Genomoviridae, while phages dominated the viral community. The dominant prokaryotic genera were Vibrio, Formosa, Aurantisolimonas, and Shewanella in the shrimp intestine, and Formosa, Aurantisolimonas, Algoriphagus, and Flavobacterium in the sediment. The viral and prokaryotic composition of the shrimp intestine and sediment were significantly different at four culture stages, and the phage communities were closely related to the prokaryotic communities. Moreover, the phage-prokaryote interactions can directly or indirectly modulate the microbial community composition and function, including auxiliary metabolic genes and closed toxin genes. The interactional analysis revealed that phages and prokaryotes had diverse coexistence strategies in the shrimp intestine and sediment microhabitats of SCPE. Collectively, our findings characterized the composition of viral communities in the shrimp intestine and cultural sediment and revealed the distinct pattern of phage-prokaryote interaction in modulating microbial community diversity, which expanded our cognization of the phage-prokaryote coexistence strategy in aquatic ecosystems from the microecological perspective and provided theoretical support for microecological prevention and control of shrimp culture health management.

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Phage and bacteria support mutual diversity in a narrowing staircase of coexistence.

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Phage and bacteria support mutual diversity in a narrowing staircase of coexistence.

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