Bioﬁlms-Promote-Altruism

Biofilms promote altruism Jan-Ulrich Kreft Correspondence Jan-Ulrich Kreft [email protected] Theoretical Biology, University of Bonn, Kirschallee 1, 53115 Bonn, Germany Received 13 October 2003 Revised 28 April 2004 Accepted 7 May 2004 The origin of altruism is a fundamental problem in evolution, and the maintenance of biodiversity is a fundamental problem in ecology. These two problems combine with the fundamental microbiological question of whether it is always advantageous for a unicellular organism to grow as fast as possible. The common basis for these three themes is a trade-off between growth rate and growth yield, which in turn is based on irreversible thermodynamics. The tra de- off create s an evolution ary alt ern ati ve between twostrate gie s: high growth yie ld at lowgrowth rate versus high growth rate at low growth yield. High growth yield at low growth rate is a case of an altruistic strategy because it increases the fitness of the group by using resources economically at the cost of decreased fitness, or growth rate, of the individual. The group-benefic ial beh avi our is adv ant ageousin thelong ter m, whe reas thehigh gro wth rate strategy is advantageous in the short term. Coexistence of species requires differences between their niches, and niche space is typically divided into four ‘axes’ (time, space, resources, predators). This neglects survival strategies based on cooperation, which extend the possibilities of coe xis ten ce, arguin g for the inclusionof coo per ati on as the fift h ‘ax is’. Here, individual-base d model simulations show that spatial structure, as in, for example, biofilms, is necessary for the origin and maintenance of this ‘primitive’ altruistic strategy and that the common belief that growth rate but not yield decides the outcome of competition is based on chemostat models and experiments. This evolutionary perspective on life in biofilms can explain long-known biofilm characteristics, such as the structural organization into microcolonies, the often-observed lack of mixing among microcolonies, and the shedding of single cells, as promoting the origin and maintenance of the altruistic strategy. Whereas biofilms enrich altruists, enrichment cultures, microbiology’s paradigm for isolating bacteria into pure culture, select for highest growth rate. INTRODUCTION In the context of evolutionary theory, altruism is defined as beh aviour tha t ben efit s oth ers whi le cos tin g sel f. In the context of human behaviour, altruism implies a concern for the welfare of other s as the motivat ion for that behavio ur, and this is how the term al tr ui sm is us ed in ever yday language. However, for evolutionary altruism, the motiva- tion, if any, for altruistic behaviour is not considered. Since ben efit s and costs are rel ati ve as we ll as loc al, alt rui stic be havi our ma y be defined more precis el y, fr om the persp ectiv e of mult i-le vel selec tion theory, as behav iour tha t inc reases the fitnes s of the group re lat ive to ot her groups while it decreases the fitness of the altruist relative to others wi thi n the gro up (S obe r & Wil son, 1998). The eco nomica l use of limiti ng res our ces is suc h a case of altruism because of a trade-off between specific growth rate (rate of biomass increase per time and biomass) and growth yield (biomass formed per amount of resource used) (Pfeiffer et al ., 2001). High growth yield, in other words, the economical use of common resources, increases group fitness. However, this can only be attained at the cost of a decreased growth rate, which decreases individual fitness. This form of altruism does not require memory of past interactions, recognition of individuals, sophisticated inter- actio ns or behav iour al reper toir es, or direc t inte racti ons between individuals. It is therefore the simplest form of altruism. Spatial structure is well known to facilitate the evolution of cooperation and altruism (see e.g. Nowak & May, 1992; Sigmund, 1994; Hofbauer & Sigmund, 1998; Hauert et al ., 200 2) . For the alt rui stic strate gy stu died her e, spa tia l structure is absolutely necessary since recognition of other individuals and their behaviour, i.e. social structure that could substitute for spatial structure, is beyond the means of bacteria. However, this requirement is easily met, because the spatial stru cture is automatica lly genera ted simply by the asexual division of immotile cells, which leads to clonal clusters. This self-organized structure merely needs to be maintained. Since the earliest forms of life were presumably immotile, asexual cells unable to recognize the individuals Abbreviations: YS, yield strategy – high growth yield at the cost of low growth rate; RS, rate strategy – high growth rate at the cost of low growth yield. 0002-6829 G 2004 SGM Printed in Great Britain 2751 Microbiology (2004), 150, 2751–2760 DOI 10.1099/mic.0.26829-0

Bioﬁlms-Promote-Altruism

Documents

Transcript of Bioﬁlms-Promote-Altruism