Cellular Innovation of the Cyanobacterial Heterocyst by the Adaptive Loss of Plasticity

Highlights

• A novel nitrogen-fixing heterocyst has evolved multiple times in Fischerella

• The envelopes of these heterocysts are less permeable than those of ancestral cells

• This is adaptive at high temperature but results in ecological specialization

• Adaptation involved loss of phenotypic plasticity and has a simple genetic basis

Summary

Cellular innovation is central to biological diversification, yet its underlying mechanisms remain poorly understood [1]. One potential source of new cellular traits is environmentally induced phenotypic variation, or phenotypic plasticity. The plasticity-first hypothesis [2, 3, 4] proposes that natural selection can improve upon an ancestrally plastic phenotype to produce a locally adaptive trait, but the role of plasticity for adaptive evolution is still unclear [5, 6, 7, 8, 9, 10]. Here, we show that a structurally novel form of the heterocyst, the specialized nitrogen-fixing cell of the multicellular cyanobacterium Fischerella thermalis, has evolved multiple times from ancestrally plastic developmental variation during adaptation to high temperature. Heterocyst glycolipids (HGs) provide an extracellular gas diffusion barrier that protects oxygen-sensitive nitrogenase [11, 12], and cyanobacteria typically exhibit temperature-induced plasticity in HG composition that modulates heterocyst permeability [13, 14]. By contrast, high-temperature specialists of F. thermalis constitutively overproduce glycolipid isomers associated with high temperature to levels unattained by plastic strains. This results in a less-permeable heterocyst, which is advantageous at high temperature but deleterious at low temperature for both nitrogen fixation activity and fitness. Our study illustrates how the origin of a novel cellular phenotype by the genetic assimilation and adaptive refinement of a plastic trait can be a source of biological diversity and contribute to ecological specialization.