The Russian Doll Model: How Bacteria Shape Successful and Sustainable Inter-Kingdom Relationships

Abstract

Successful inter-kingdom relationships are based upon a dynamic balance between defense and cooperation. A certain degree of competition is necessary to guarantee life spread and development. On the other hand, cooperation is a powerful tool to ensure a long lasting adaptation to changing environmental conditions and to support evolution to a higher level of complexity. Bacteria can interact with their (true or potential) parasites (i.e., phages) and with their multicellular hosts. In these model interactions, bacteria learnt how to cope with their inner and outer host, transforming dangerous signals into opportunities and modulating responses in order to achieve an agreement that is beneficial for the overall participants, thus giving rise to a more complex "organism" or ecosystem. In this review, particular attention will be addressed to underline the minimal energy expenditure required for these successful interactions [e.g., moonlighting proteins, post-translational modifications (PTMs), and multitasking signals] and the systemic vision of these processes and ways of life in which the system proves to be more than the sum of the single components. Using an inside-out perspective, I will examine the possibility of multilevel interactions, in which viruses help bacteria to cope with the animal host and bacteria support the human immune system to counteract viral infection in a circular vision. In this sophisticated network, bacteria represent the precious link that insures system stability with relative low energy expenditure.

Should Bacteriophages Be Classified as Parasites or Predators?

“…The permanent infection, also called the chronic cycle ( Pessione 2020 ), generally resembles the lytic cycle; however, in this case, propagating bacteriophage does not kill its bacterial host (at least not immediately and directly) but progeny virions of the bacteriophage continuously formed are released through a cell envelope without killing the bacterium. Interestingly, this cycle causes a lower growth rate of the host bacterial cell because part of the cell energy is directed to phage functions ( Munson-McGee et al 2018 ).…”

“…Apart from the direct use of phages infecting pathogenic bacteria to patients, it is also essential to consider their application to control single- or mixed-species biofilms in therapy and protection of medical devices or food ( Mgomi et al 2021 ; Tian et al 2021 ; Topka-Bielecka et al 2021 ). Importantly, bacteriophages efficiently modulate the human microbiome, which has considerable effects on the physiology of the whole human organism ( Pessione 2020 ; Duan et al 2021 ; Hsu et al 2021 ; Zhang et al 2021 ). On the other hand, some bacteriophages encode toxins and other virulence factors, which if produced by bacterial cells after prophage induction, can cause severe human diseases ( Casas and Maloy 2011 ; Łoś et al 2011 ; Boyd 2012 ).…”

The Less Expensive Choice: Bacterial Strategies to Achieve Successful and Sustainable Reciprocal Interactions

“…Vesicles are present in Gram-negative and Gram-positive bacteria and can originate both in the outer ( Manning and Kuehn, 2011 ) and in the cytoplasmic membrane ( Lee et al, 2009 ). The role of lysogenic phages in membrane vesicle biogenesis has been ascertained and recently reviewed ( Pessione, 2020 ). The system, used to translocate the transported molecules directly inside the target cell by means of membrane fusion, proved to be more efficient than simple metabolite secretion since inside the vesicles the different compounds are protected both from enzymatic degradation and from host factors (for instance, quorum quenching in case of symbiont bacteria) ( Figure 3b ).…”

Bacteriophages—Dangerous Viruses Acting Incognito or Underestimated Saviors in the Fight against Bacteria?

“…The chronic mode (also called a permanent infection) resembles the lytic mode, but newly formed virions are released without killing 2 of 15 the bacterial host cell, or at least not killing it immediately. In fact, the host eventually dies, but due to exhaustion of the energy sources rather than to cell lysis [6].…”