Privatization of public goods can cause population decline

Abstract

5Microbes commonly deploy a risky strategy to acquire nutrients from their environment, involving the 6 production of costly public goods that can be exploited by neighbouring individuals. Why engage in 7 such a strategy when an exploitation-free alternative is readily available whereby public goods are 8 kept private? We address this by examining metabolism of Saccharomyces cerevisiae both in its 9 native form and by creating a novel three-strain synthetic community deploying different strategies of 10 sucrose metabolism. Public-metabolisers digests resources externally, private-metabolisers 11 internalise resources before digestion, and cheats avoid the metabolic costs of digestion but exploit 12 external products generated by competitors. A combination of mathematical modelling and ecological 13 experiments reveal that private-metabolisers invade and take over an otherwise stable community of 14 public-metabolisers and cheats. However, owing to the reduced growth rate of private-metabolisers 15 and population bottlenecks that are frequently associated with microbial communities, privatising 16 public goods can become unsustainable, leading to population decline. 17 have been described as 'private goods' 17 . However, such 'private goods' do not overcome the 51 evolutionary incentive for cheating 43 , as is the case with our definition. 52We assess the benefits of public goods metabolism using a combination of mathematical modelling 53 and synthetic ecology. We focus on different strategies that Saccharomyces cerevisiae deploys to 54 metabolise disaccharides as an ideal exemplar. S. cerevisiae can metabolise the disaccharides 55 maltose and sucrose, which have the same molecular formula (C12H22O11) but differ in their 56 constituent monosaccharides: maltose consists of two glucose molecules whereas sucrose is one 57 glucose and one fructose molecule. Disaccharides are broken down into their constituent 58 monosaccharides, before being catabolised by the glycolytic pathway. Curiously, considering the 59 similarities, S. cerevisiae deploys different strategies for their consumption. Maltose is internalised 60 through maltose transporters before being hydrolysed by maltase, whereas sucrose is hydrolysed 61 externally by an extracellular invertase, and the resulting monosaccharides are subsequently 62 internalised 44 . 63By comparing features of wild type public sucrose metabolism and private maltose metabolism when 64 grown alone (axenically), we demonstrate how public and private metabolism by S. cerevisiae can 65 provide different environment-dependent selective benefits. A number of important differences 66 emerge. Growth on maltose was less hampered by diminishing resource concentrations than growth 67 on sucrose. However, sucrose metabolism facilitated a higher growth rate than maltose metabolism 68 when population density and resource concentrations were sufficiently high. 69To understand how ecological interactions between such contrasting metabolic strategies influence 70 their evolutionary potential, we d...

Universality of dissipative self-assembly from quantum dots to human cells

“…Eventually, growth saturates due to the finite extent over which flows are induced by the laser and also because the entities are depleted from the vicinity of the aggregates. These mechanisms result in a sigmoidal growth curve, which is commonly observed in diverse complex, dynamic adaptive systems [37][38][39] .…”

Predicting microbial growth dynamics in response to nutrient availability

“…Therefore, understanding and predicting microbial population dynamics is a key challenge for the fields of ecology, evolution, public health, and biotechnology. Mathematical models of microbial growth and metabolism form the foundation of many predictions regarding competition [7][8][9], metabolic interactions [10], cooperation [11][12][13][14][15], and diversification [16,17] within microbial communities, as well as product formation and its optimisation for use in biotechnology [18,19].…”

Coexisting with cheaters: Microbial exoenzyme production as a snowdrift game model

“…This trend of ever-decreasing enzyme production for short-terms growth benefits eventually causes the population to drift to extinction. In nature, we assume that public good producer populations are driven by selection towards a lower production of the public good, as a result of intraspecific competition (Morris, Lenski and Zinser, 2012;Sachs and Hollowell, 2012;Lindsay, Pawlowska and Gudelj, 2019). We propose that the ESS-e * m effect in the producer monoculture, imposed on the enzyme producer's abundance (Figure 2B), would not result in extinction in nature if the public good is crucial for survival and has no alternatives.…”