Scanty microbes, the ‘symbionelle’ concept

Mutualistic symbiosis occurs when two different species interact closely with each other and benefit from living and working together. However, not all symbiotic associations are of mutual benefit because there are also forms of parasitism (when one organism benefits but the other is adversely affected) and commensalism (when only one of the organisms involved in the association benefits, but the other is not affected); notwithstanding, the very fact that specific entities can exist together means that natural selection may guide them to live with each other. Endosymbiosis is a special case of symbiosis in which one partner, generally a prokaryote symbiont, lives sequestered inside specialized eukaryotic cells called bacteriocytes. The notion of microbes becoming organelles of eukaryotic systems through evolution has been widely accepted because Lynn Margulis put forward her serial endosymbiotic theory of eukaryotic cell evolution (Margulis, 1993). Indeed, this is the origin of mitochondria and chloroplasts. There is compelling evidence to support that these two eukaryotic organelles are the product of symbiotic events between prokaryotes and primitive eukaryotes (Latorre et al., 2011). Their original alpha-proteobacterial (mitochondria ancestor) and cyanobacterial (chloroplast ancestor) genomes have been drastically reduced, with a portion of the protein-encoded genes and even RNA genes being transferred to the eukaryotic nuclear genome. Other genes have simply been lost, and their function replaced by the hosts. Since the proposal of these two canonical endosymbioses, symbiotic associations between prokaryotes and unicellular and multicellular eukaryotes have been documented in practically every major branch of the tree of life, which reinforces the role played by symbiosis in the emergence of evolutionary innovations (Moya et al., 2008). Endosymbiosis in insects is a captivating example of the aforementioned phenomenon. Insects are particularly well suited to establishing intracellular symbiosis with bacteria, which provide them with the metabolic capabilities they lack and enable them to live in almost any environment. At present, there are a number of well-documented cases of insect endosymbionts at different stages of symbiotic integration (Fig. 1). Insect endosymbiosis commonly consists of an obligate mutualistic association, where bacteria produce essential nutrients that are absent in the insect’s diet, and the insect, in turn, provides the bacteria with a safe environment and a permanent food supply (Baumann, 2005). These endosymbiotic bacteria are vertically transmitted across host generations. Their metabolic role is renowned, and most insect endosymbiotic systems are largely convergent towards these functions regardless of the lifestyle or genomic repertoire of their free-living ancestor (López-Sánchez et al., 2008; McCutcheon et al., 2009; McCutcheon and Moran, 2010; Sabree et al., 2013).Anew symbiotic relationship, which represents a source of novel complexity, has to overcome the obvious problem posed by the fact that both partners must be able to survive together despite differences in biology, particularly generation times and reproduction. Moreover, considering that these organisms generally possess different population genetics and are under different evolutionary pressures, they need to establish a certain trade-off to acquire the evolutionary novelty represented by their stable coexistence (Delaye and Moya, 2010; McCutcheon and Moran, 2012). Thus, important genetic and biochemical modifications are required in these bacteria compared with their free-living state. The eukaryotic host, on the other hand, must develop ways of controlling the bacterial population, engulfing them in specialized cells –the aforesaid bacteriocytes – and/or changing immune responses to recognize these bacteria as non-pathogenic. One of the most important and well-known features of endosymbiotic bacteria is that they provide extreme examples of genomic shrinkage by undergoing a process called the ‘genomic reduction syndrome’. Hence, prokaryotic genomes of endosymbionts are examples of a particular type of naturally evolved minimal cell, with insect Received 1 July, 2013; revised 11 July, 2013; accepted 18 July, 2013. *For correspondence. E-mail andres.moya@uv.es; Tel. (+34) 96 354 3480; Fax (+34) 96 354 3670. bs_bs_banner