Implications of streamlining theory for microbial ecology

Abstract

Whether a small cell, a small genome or a minimal set of chemical reactions with self-replicating properties, simplicity is beguiling. As Leonardo da Vinci reportedly said, 'simplicity is the ultimate sophistication'. Two diverging views of simplicity have emerged in accounts of symbiotic and commensal bacteria and cosmopolitan free-living bacteria with small genomes. The small genomes of obligate insect endosymbionts have been attributed to genetic drift caused by small effective population sizes (N e ). In contrast, streamlining theory attributes small cells and genomes to selection for efficient use of nutrients in populations where N e is large and nutrients limit growth. Regardless of the cause of genome reduction, lost coding potential eventually dictates loss of function. Consequences of reductive evolution in streamlined organisms include atypical patterns of prototrophy and the absence of common regulatory systems, which have been linked to difficulty in culturing these cells. Recent evidence from metagenomics suggests that streamlining is commonplace, may broadly explain the phenomenon of the uncultured microbial majority, and might also explain the highly interdependent (connected) behavior of many microbial ecosystems. Streamlining theory is belied by the observation that many successful bacteria are large cells with complex genomes. To fully appreciate streamlining, we must look to the life histories and adaptive strategies of cells, which impose minimum requirements for complexity that vary with niche.

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

“…That is, sequenced bacteria with large genomes tend to comprise a significantly larger proportion of soil bacterial communities. On average, the genomes of soil prokaryotes are larger than those inhabiting aquatic ecosystems 27 or the human gut 28 . These relatively large genomes are thought to provide soil-dwelling bacteria with a more diverse genetic inventory to enhance survival in conditions where resources are diverse, but sparse 29,30 .…”

“…A similar pattern has been observed in aquatic systems, where uncultivated taxa often have smaller genomes than cultivated taxa 31 . Because most genomic information is derived from cultivated bacterial taxa, the lack of genomic information from bacteria with compact genomes may stem from challenges associated with culturing taxa with reduced genomes 27 .…”

“…The effect of genetic drift on microbes with a small N e and low recombination rates, such as endosymbiotic bacteria, leads to the accumulation of deleterious mutations and subsequent loss of genetic material, which is typically identifiable in genomes by the presence of numerous pseudogenes and large noncoding intergenic regions 40 . In contrast, free-living organisms with a large N e are thought to undergo 'streamlining' selection to minimize genome size 27,40 . The genome-streamlining hypothesis proposes that, in large bacterial populations, reduced genome complexity is a trait under natural selection, especially in environments where nutrients can be sparse and periodically limit growth 27 .…”

“…In contrast, free-living organisms with a large N e are thought to undergo 'streamlining' selection to minimize genome size 27,40 . The genome-streamlining hypothesis proposes that, in large bacterial populations, reduced genome complexity is a trait under natural selection, especially in environments where nutrients can be sparse and periodically limit growth 27 . The abundance, putative auxotrophies ( Supplementary Fig.…”

“…U. copiosus genome (such as large numbers of pseudogenes or unusually large intergenic spaces). Although most contemporary free-living organisms with streamlined genomes inhabit aquatic environments 27,41 , compared to these aquatic environments, soil is more heterogeneous 42 , has greater overall microbial diversity 43 and slower carbon turnover 44 . Therefore, the functional complexity required by soil microbes to succeed within a given niche is probably large relative to that required by aquatic microbes.…”