Surfacing views of biofilm biology

Contained within this issue of Trends in Microbiology is a collection of review articles focusing on various aspects of biofilm biology. For several years now microbiologists have been increasingly turning their attention to the study of surface-associated microbial communities. As a consequence, the scientific community has seen an explosion in the number of articles that describe some new aspect of the multifarious existence that microbes lead on surfaces. The expanding exploration of biofilm biology has led to an ever increasing appreciation that the biological properties of biofilms are as diverse as the organisms that constitute them and the myriad of environments under which they are known to form.The fact that microbes appear to grow predominantly on surfaces has been recognized by microbiologists for many decades. Thus, one might have suspected that biofilms would have been the subject of intense study since the early days of our discipline. What led to the fact that biofilms were not a focus of microbiologists' attention for so many years? No doubt the ‘pure culture’ tradition, in which medical microbiology is so deeply steeped, and the ostensible cellular homogeneity of a microbial population growing in exponential phase, greatly biased researchers towards the study of planktonic populations of single microbial species. And thank goodness for that fact! Where would we be today without the legacy of more than half a century of studies of colony-purified strains grown in defined artificial media and investigated through the power of molecular genetics? So deeply engrained were we in these traditions that it is harder to explain just what events or changes in the mindset of the microbiologist were most responsible for the explosion in the interest in biofilm biology that has occurred in the past decade. The problems that recalcitrant biofilms wreak on medical devices must have contributed to the appreciation that surface-associated microbes have a physiology different from that of planktonic cells. As did the recognition that intercellular chemical signaling is the rule rather than the exception amongst microbial populations. Regardless of the reasons, there is little doubt that biofilm studies now command much attention among microbial scientists.How has our knowledge been advanced as a consequence of this increased research? Where do we stand as a community of scientists vis-a-vis biofilms? One of the ongoing debates in biofilm biology centers around the question of whether or not biofilm formation constitutes a developmental process in which cells commit to a change in lifestyle through a programmed cascade of changes in gene expression. Do biofilms form and acquire their individual architecture simply as a result of the physicochemical properties of the particular environments in which they form? The initial view that biofilm structures could be wholly explained by nutrient-limited microbial growth on a surface is slowly giving way to a view based largely on results that stem from molecular genetic analyses, of biofilm growth that involves regulatory processes through which the organisms adjust to and commit to growth on a surface. Still, it is not entirely clear just how many of the properties of any given biofilm are dictated by developmental programs of the constituent organisms and how many are dictated by the environmental conditions in which the biofilm is growing. On a ‘micro’ scale, this is a case of the age-old nature versus nurture debate. And, as it will become apparent from reading the reviews, biofilm formation involves the interaction of environmental conditions and the microbes' ability to respond to these.The notion of the ‘universality of biofilms’ has also evolved in two important ways as a result of the increased interest in studying biofilms. On the one hand, the concept that a limited number of microbial species were ‘good biofilm formers’ has been supplanted by the sense that biofilm formation is most likely a universal feature of microbes, a feature that can be discovered through the use of undomesticated microbial strains and testing under diverse environmental conditions. On the other hand, the initial striving by numerous investigators to find universal biofilm-related genes and/or attributes, such as the search for the commonalities of all biofilms, has subsided and given way to a view that embraces the diversity of the microbial world. In a similar way that the study over many decades of diverse microbes growing in liquid culture gave us a glimpse of the amazingly diverse metabolic capabilities of different microbes, the study of different biofilms has opened our eyes to other manifestations of diversity. Although it appears that all microbes can make biofilms, they do so in ways that are idiosyncratic to the particular strain and environmental conditions.As will become apparent to the reader of the reviews contained herein, there are many insights regarding the vast diversity of microbial physiology that have been gleaned, at least in part, from the study of surface-associated communities. Communication between cells, interactions among species, expression of new phenotypic traits, and the molecular mechanisms underlying the switch from a planktonic to a sessile existence, are all topics that are extensively covered by the authors of this collection of reviews. What one ‘takes home’ after even a brief acquaintance with biofilms is that there is something striking about microbes living on surfaces. Invariably, microbes carry out fascinating, and often unexpected, processes when presented with the greater organizing potential afforded by a surface. Once on a surface, microbial cells can begin long-term relationships with each other; therein lies the transition from unicellularity to multicellularity. As this collection of reviews reveals, analyses of microbial activities on surfaces have already provided, and will continue to provide, new insights into the wonderful diversity of the microbial world.