Super life – how and why ‘cell selection’ leads to the fastest‐growing eukaryote

Abstract

What is the highest possible replication rate for living organisms? The cellular growth rate is controlled by a variety of processes. Therefore, it is unclear which metabolic process or group of processes should be activated to increase growth rate. An organism that is already growing fast may already have optimized through evolution all processes that could be optimized readily, but may be confronted with a more generic limitation. Here we introduce a method called ‘cell selection’ to select for highest growth rate, and show how such a cellular site of ‘growth control’ was identified. By applying pH‐auxostat cultivation to the already fast‐growing yeast Kluyveromyces marxianus for a sufficiently long time, we selected a strain with a 30% increased growth rate; its cell‐cycle time decreased to 52 min, much below that reported to date for any eukaryote. The increase in growth rate was accompanied by a 40% increase in cell surface at a fairly constant cell volume. We show how the increase in growth rate can be explained by a dominant (80%) limitation of growth by the group of membrane processes (a 0.7% increase of specific growth rate to a 1% increase in membrane surface area). Simultaneous activation of membrane processes may be what is required to accelerate growth of the fastest‐growing form of eukaryotic life to growth rates that are even faster, and may be of potential interest for single‐cell protein production in industrial ‘White’ biotechnology processes.

Physiological diversity within the kluyveromyces marxianus species

“…In addition, this species is able to grow at temperatures up to 45°C (Rouwenhorst et al 1988;Steensma et al 1988), possesses a high capacity of converting substrate into biomass (Bellaver et al 2004;Fonseca et al 2007) and the highest specific growth rate among eukaryotes (Groeneveld et al 2009). Furthermore, some strains in the species show dimorphism, a phenomenon that is described in a few yeast species, including the widely studied Saccharomyces cerevisiae (Hill and Robinson 1988), and the less conventional Wickerhamomyces anomalus (Sundhagul and Hedrick 1966).…”

Fermentative production of ribonucleotides from whey by Kluyveromyces marxianus: effect of temperature and pH

“…These studies revealed the maximum ribonucleotides production by K. marxianus in whey fermentation under fed-batch or continuous cultivations after maintaining a logarithmic growth phase of K. marxianus. The cellular growth rate of any microorganism is controlled by a variety of factors involved in the metabolic processes (Groeneveld et al 2009). It is therefore difficult to explain that which metabolic process or combined processes are responsible for the hikes in growth.…”

“…K. marxianus is known as fast growing eukaryote showing its potential for the application in industrial biotechnology processes. Groeneveld et al (2009) demonstrated a "cell selection method" to reveal the effect of metabolic process or pool of metabolic processes on growth control of K. marxianus by applying pH-auxostat cultivation. They were able to select a strain with a 30% increased growth rate by the cell selection method reporting decreased cell-cycle time to 52 min, much below that reported to date for any eukaryote.…”

The renaissance of continuous culture in the post-genomics age

“…The power of this type of continuous culture was demonstrated recently by Groeneveld et al [71] in selecting for increased specific growth rate of the yeast Kluyveromyces marxianus. Other applications include the investigation of sulphate reduction under acidic conditions favourable for metal bioleaching [17].…”

“…Groeneveld et al [71] made use of pH auxostats to select for adapted strains of Kluyveromyces marxianis that had increased specific growth rates. While this yeast is notable among eukaryotic microorganisms in displaying a high l max (0.6 h -1 ) this is substantially lower than that of the most rapidly growing prokaryote (ca.…”