The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss

Abstract

<jats:title>ABSTRACT</jats:title><jats:p>Reductive genomic evolution, driven by genetic drift, is common in endosymbiotic bacteria. Genome reduction is less common in free-living organisms, but it has occurred in the numerically dominant open-ocean bacterioplankton<jats:italic>Prochlorococcus</jats:italic>and “<jats:italic>Candidatus</jats:italic>Pelagibacter,” and in these cases the reduction appears to be driven by natural selection rather than drift. Gene loss in free-living organisms may leave them dependent on cooccurring microbes for lost metabolic functions. We present the Black Queen Hypothesis (BQH), a novel theory of reductive evolution that explains how selection leads to such dependencies; its name refers to the queen of spades in the game Hearts, where the usual strategy is to avoid taking this card. Gene loss can provide a selective advantage by conserving an organism’s limiting resources, provided the gene’s function is dispensable. Many vital genetic functions are leaky, thereby unavoidably producing public goods that are available to the entire community. Such leaky functions are thus dispensable for individuals, provided they are not lost entirely from the community. The BQH predicts that the loss of a costly, leaky function is selectively favored at the individual level and will proceed until the production of public goods is just sufficient to support the equilibrium community; at that point, the benefit of any further loss would be offset by the cost. Evolution in accordance with the BQH thus generates “beneficiaries” of reduced genomic content that are dependent on leaky “helpers,” and it may explain the observed nonuniversality of prototrophy, stress resistance, and other cellular functions in the microbial world.</jats:p>

Torn apart and reunited: impact of a heterotroph on the transcriptome of Prochlorococcus

“…In addition, we also observed a significant increase in the abundance of catalase-peroxidase transcripts (Table 4). This is consistent with the 'Black Queen' hypothesis (Morris et al, 2012), which posits that the evolutionary loss of the catalase gene in Prochlorococcus was facilitated by the ability of heterotrophs to provide this 'leaky' function. Although it is unclear which, if any, of these heterotroph transcriptomic responses were specific to co-culture with Prochlorococcus as opposed to changes owing to stresses, growth or simply changes in the nutrient environment, these results support the hypothesis that the chemical conversation in the co-culture was two-sided.…”

“…This phenomenon is attributable at least in part to the role of heterotrophs in reducing the levels of toxic reactive oxygen species such as hydrogen peroxide (Morris et al, 2008(Morris et al, , 2011. This is thought to compensate for the absence of catalase in the Prochlorococcus genome, indicating that interspecies interactions have clearly influenced the evolutionary selective pressures and processes acting upon this group of organisms (Morris et al, 2012). Heterotrophs in Prochlorococcus cultures in turn receive photosynthetically fixed organic carbon and other nutrients supplied by Prochlorococcus; indeed, many heterotrophs thrive in Prochlorococcus co-cultures in the absence of any added carbon.…”

Genome reduction in an abundant and ubiquitous soil bacterium ‘Candidatus Udaeobacter copiosus’

“…Furthermore, many of the amino acids and vitamins Ca. U copiosus appears unable to synthesize are involved in synergistic growth 47 and may be supplied by other microbes as common community goods 48 . Based on the few spartobacterial isolates that have been cultivated 11 , culture-independent studies 10,49 and the genomic data presented here, we speculate that Ca.…”

Transcriptional response of Prochlorococcus to co-culture with a marine Alteromonas: differences between strains and the involvement of putative infochemicals

“…Several recent studies have shown that co-occurring heterotrophic bacteria can both enhance and inhibit the growth of Prochlorococcus in laboratory co-cultures (Morris et al, 2008;Sher et al, 2011). Furthermore, such interactions may have significant effects on the viability of Prochlorococcus in the oceans, for example through scavenging by heterotrophic bacteria of reactive oxygen species (ROS) produced by Prochlorococcus (Morris et al, 2011(Morris et al, , 2012. Finally, both Prochlorococcus and related Synechococcus strains have been shown to produce a wide diversity of ribosomally-synthesized peptides, which are then post-translationally modified to form lanthipeptides and microcins (Li et al, 2010;Paz-Yepes et al, 2013).…”