Flagellar phenotypic plasticity in volvocalean algae correlates with Péclet number

Abstract

Flagella-generated fluid stirring has been suggested to enhance nutrient uptake for sufficiently large micro-organisms, and to have played a role in evolutionary transitions to multicellularity. A corollary to this predicted size-dependent benefit is a propensity for phenotypic plasticity in the flow-generating mechanism to appear in large species under nutrient deprivation. We examined four species of volvocalean algae whose radii and flow speeds differ greatly, with Péclet numbers (Pe) separated by several orders of magnitude. Populations of unicellular Chlamydomonas reinhardtii and one-to eight-celled Gonium pectorale (Pe 0.1-1) and multicellular Volvox carteri and Volvox barberi (Pe 100) were grown in diluted and undiluted media. For C. reinhardtii and G. pectorale, decreasing the nutrient concentration resulted in smaller cells, but had no effect on flagellar length and propulsion force. In contrast, these conditions induced Volvox colonies to grow larger and increase their flagellar length, separating the somatic cells further. Detailed studies on V. carteri found that the opposing effects of increasing beating force and flagellar spacing balance, so the fluid speed across the colony surface remains unchanged between nutrient conditions. These results lend further support to the hypothesized link between the Péclet number, nutrient uptake and the evolution of biological complexity in the Volvocales.

Coordinated beating of algal flagella is mediated by basal coupling

“…The alga Volvox carteri (VC) is perhaps the smallest colonial organism to exhibit cellular division of labor (13). Adult spheroids possess two cell types: Large germ cells interior of an extracellular matrix grow to form new colonies, whereas smaller somatic cells form a dense surface covering of flagella protruding into the medium, enabling swimming.…”

The Evolutionary Ecology of Multicellularity: The Volvocine Green Algae as a Case Study

“…2). Sedimentation speeds were higher for G. pectorale compared to C. reinhardtii in Solari et al (2006a;9.5 μm/sec vs. 1.4 μm/sec) and in Solari et al (2011; 10 μm/sec in full and 8.9 μm/sec in diluted medium vs. 6.5 μm/sec in full and 3.7 μm/sec in diluted medium).…”

“…Complementing the low Pe calculation on G. pectorale, it was reported in Solari et al (2011) that two Volvox species with thousand of cells made an investment into collective flagellar beating during nutrient deprivation, but under those same conditions C. reinhardtii and G. pectorale did not.…”

“…Furthermore, when swimming speeds in synchronized populations at 1 and 3 h into the light cycle (Solari et al 2006a) and in full and diluted medium (Solari et al 2011) was measured, the average upward swimming speed of G. pectorale colonies was even lower than that of the unicellular C. reinhardtii. In Solari et al (2006a), G. pectorale upward swimming speeds were 32.5 μm/sec vs. 38 μm/sec for C. reinhardtii (most G. pectorale colonies in this experiments were 8-celled), and in Solari et al (2011), G. pectorale upward swimming speeds were 33 μm/sec in full and 37 μm/sec in diluted medium vs. 43 μm/sec and 54 μm/sec for C. reinhardtii (most G. pectorale colonies in this experiments were 4-celled). Moreover, the plate colony design of G. pectorale did not slow sinking (Fig.…”

Swimming like algae: biomimetic soft artificial cilia

“…A movie was taken of a single Volvox colony in the second half of its 48 h life cycle. A schematic of this life cycle is shown in Solari et al [26]. The cilium studied in this paper was close to the anterior pole of the Volvox colony.…”