Experimental evidence that evolution by niche construction affects dissipative ecosystem dynamics

Abstract

Evolution by niche construction occurs when organism-mediated modification of the environment causes an evolutionary response. Physicists have postulated that evolution in general, and evolution mediated via feedbacks between organisms and their environment in particular (i.e. evolution by niche construction), could increase the capacity of biological systems to dissipate free energy in an open thermodynamic system, and help them maintain a state far from thermodynamic equilibrium. Here, we propose using the bacterium Pseudomonas fluorescens (strain SBW25) as a model system to experimentally test theories in both evolutionary biology (e.g. niche construction) and physics (e.g. dissipative systems theory). P. fluorescens rapidly and predictably evolves multiple strategies for exploiting oxygen in unmixed culture flasks. This evolutionary dynamic is mediated by feedbacks between the modification of the oxygen gradient by P. fluorescens and the ecological and evolutionary responses of Pseudomonas to modified environmental conditions. To confirm this, we experimentally manipulated two aspects of the system that influence the strength of the feedback between P. fluorescens and oxygen gradients in the system. First, we inhibited the metabolism of the strain used to inoculate the cultures, and, second, we disturbed the formation of mats at the air-liquid interface. Overall, we found convincing experimental evidence of evolution by niche construction, and conclude that this study system is amenable to experimental investigations of both niche construction and dissipative systems theory.

An enormous potential for niche construction through bacterial cross-feeding in a homogeneous environment

“…Prominent examples of niche construction include animals that construct artifacts such as webs, nests and burrows [ 24 ]; earthworms and plants that alter the fertility, humidity and chemical composition of soil [ 28 , 30 , 31 ]; and bacteria that construct biofilms and excrete antibiotics as well as metabolic by-products [ 32 ]. Constructed niches can affect evolution even on the short time scales of experimental evolution, where populations of Pseudomonas fluorescens become dependent on their own modifications of their chemical environment [ 33 , 34 ].…”

Physical Constraints on Global Social-Ecological Energy System

“…In fact, the evolution of societal complexity depends critically on energy availability [60,61]. In particular, SES complexification leads to higher energy costs and dispersion, which is used by SES to maintain the existing thermodynamic disequilibrium and structure [62]. This co-evolutionary pattern is indirectly confirmed by trends reported in Figures 2, 4 and 5.…”

Community biofilm-formation, stratification and productivity in serially-transferred microcosms

“…Higher levels of enrichment at the top across final-transfer communities compared with the soil-wash inoculum suggest niche selection for strains able to compete efficiently in high-O2 conditions has occurred, underlying the fact that in our model system O2 is growth-limiting in both static and shaken microcosms. Ecological filtering has not been strong enough to reduce colonisation of the low-O2 region, despite the fact that biofilms are known to steepen the O2 gradient formed in static microcosms (Koza et al 2011;Loudon et al 2016). This may be because many strains are able to compete effectively in both regions because sufficient O2 remains in this region to support some level of growth or alternative electro-acceptors are used by some community members.…”

“…In the context of SBW25 spatially-structured static microcosms, the high-O2 region represents an un-occupied niche ready for colonisation by biofilmcompetent or aerotaxic community members rather than an ecological opportunity in the sense of adaptive radiation (Wellborn & Langerhans, 2014). We expect that communities established from environmental samples in the same type of static microcosms used for SBW25 would develop O2 gradients as rapidly as SBW25 colonists (Koza et al 2011;Loudon et al 2016) and also produce A-L interface biofilms. In such community microcosms, we hypothesize competition for limited resources will drive changes in community structure and biofilms and maximise productivity through an increase in the abundance of successful competitors and a reduction in functional redundancy (Nadell et al 2009;Cavaliere et al 2017) (even in a two-species system, interactions can affect productivity, Zhang et al 2012, and biofilm rheology is determined by the fastest-growing member, Abriat et al 2020).…”