Microbes are generally thought of as unicellular organisms, but we know that many microbes live as parts of biofilms—complex, surface-attached microbial communities numbering millions of cells. Some authors have recently argued in favour of reconceiving biofilms as biological entities in their own right. In particular, some have claimed that multispecies biofilms are evolutionary individuals : 10126–10132 2015). Against this view, I defend the conservative consensus that selection acts primarily upon microbial cells.

This paper examines David Hull’s and Peter Godfrey-Smith’s accounts of biological individuality using the case of biofilms. Biofilms fail standard criteria for individuality, such as having reproductive bottlenecks and forming parent-offspring lineages. Nevertheless, biofilms are good candidates for individuals. The nature of biofilms shows that Godfrey-Smith’s account of individuality, with its reliance on reproduction, is too restrictive. Hull’s interactor notion of individuality better captures biofilms, and we argue that it offers a better account of biological individuality. However, Hull’s notion of (...) interactor needs more precision. We suggest some ways to make Hull’s notion of interactor and his account of individuality more precise. Generally, we maintain that biofilms are a good test case for theories of individuality, and a careful examination of biofilms furthers our understanding of biological individuality. (shrink)

Biofilms can be viewed as tissue‐like structures in which microorganisms are organized in a spatial and functional sophisticated manner. Biofilm formation requires the orchestration of a highly integrated network of regulatory proteins to establish cell differentiation and production of a complex extracellular matrix. Here, we discuss the role of the essential Bacillus subtilis biofilm activator RemA. Despite intense research on biofilms, RemA is a largely underappreciated regulatory protein. RemA forms donut‐shaped octamers with the potential to assemble into dimeric (...) superstructures. The presumed DNA‐binding mode suggests that RemA organizes its target DNA into nucleosome‐like structures, which are the basis for its role as transcriptional activator. We discuss how RemA affects gene expression in the context of biofilm formation, and its regulatory interplay with established components of the biofilm regulatory network, such as SinR, SinI, SlrR, and SlrA. We emphasize the additional role of RemA played in nitrogen metabolism and osmotic‐stress adjustment. (shrink)

Doolittle :351–378, 2013) and Ereshefsky and Pedroso argue that selection can act at the level of biofilms and other microbial communities. Clarke is skeptical and argues that selection acts on microbial cells rather than microbial communities. Her main criticism is that biofilms lack one of the ingredients required for selection to operate: heritability. This paper replies to her concern by elaborating how biofilm-level traits can be inheritable.

Both physiological and evolutionary criteria of biological individuality are underpinned by the idea that an individual is a functionally integrated whole. However, a precise account of functional integration has not been provided so far, and current notions are not developed in the details, especially in the case of composite systems. To address this issue, this paper focuses on the organisational dimension of two representative associations of prokaryotes: biofilms and the endosymbiosis between prokaryotes. Some critical voices have been raised against the (...) thesis that biofilms are biological individuals. Nevertheless, it has not been investigated which structural and functional obstacles may prevent them from being fully integrated physiological or evolutionary units. By contrast, the endosymbiotic association of different species of prokaryotes has the potential for achieving a different type of physiological integration based on a common boundary and interlocked functions. This type of association had made it possible, under specific conditions, to evolve endosymbionts into fully integrated organelles. This paper therefore has three aims: first, to analyse the organisational conditions and the physiological mechanisms that enable integration in prokaryotic associations; second, to discuss the organisational differences between biofilms and prokaryotic endosymbiosis and the types of integration they achieve; finally, to provide a more precise account of functional integration based on these case studies. (shrink)

The importance of electrical signalling in bacteria is an emerging paradigm. Bacillus subtilis biofilms exhibit electrical communication that regulates metabolic activity and biofilm growth. Starving cells initiate oscillatory extracellular potassium signals that help even the distribution of nutrients within the biofilm and thus help regulate biofilm development. Quorum sensing also regulates biofilm growth and crucially there is convergence between electrical and quorum sensing signalling axes. This makes B. subtilis an interesting model for cell signalling research. SpoOF (...) is predicted to act as a logic gate for signalling pathway convergence, raising interesting questions about the functional nature of this gate and the relative importance of these disparate signals on biofilm behaviour. How is an oscillating signal integrated with a quorum signal? The model presented offers rich opportunities for future experimental and theoretical modelling research. The importance of direct cell‐to‐cell electrical signalling in prokaryotes, so characteristic of multicellular eukaryotes, is also discussed. (shrink)

This paper focuses on physiological integration in multicellular systems, a notion often associated with biological individuality, but which has not received enough attention and needs a thorough theoretical treatment. Broadly speaking, physiological integration consists in how different components come together into a cohesive unit in which they are dependent on one another for their existence and activity. This paper argues that physiological integration can be understood by considering how the components of a biological multicellular system are controlled and coordinated in (...) such a way that their activities can contribute to the maintenance of the system. The main implication of this perspective is that different ways of controlling their parts may give rise to multicellular organizations with different degrees of integration. After defining control, this paper analyses how control is realized in two examples of multicellular systems located at different ends of the spectrum of multicellularity: biofilms and animals. It focuses on differences in control ranges, and it argues that a high degree of integration implies control exerted at both medium and long ranges, and that insofar as biofilms lack long-range control (relative to their size) they can be considered as less integrated than other multicellular systems. It then discusses the implication of this account for the debate on physiological individuality and the idea that degrees of physiological integration imply degrees of individuality. (shrink)

The article proposes to further develop the ideas of the Extended Evolutionary Synthesis by including into evolutionary research an analysis of phenomena that occur above the organismal level. We demonstrate that the current Extended Synthesis is focused more on individual traits (genetically or non-genetically inherited) and less on community system traits (synergetic/organizational traits) that characterize transgenerational biological, ecological, social, and cultural systems. In this regard, we will consider various communities that are made up of interacting populations, and for which the (...) individual members can belong to the same or to different species. Examples of communities include biofilms, ant colonies, symbiotic associations resulting in holobiont formation, and human societies. The proposed model of evolution at the level of communities revises classic theorizing on the major transitions in evolution by analyzing the interplay between community/social traits and individual traits, and how this brings forth ideas of top-down regulations of bottom-up evolutionary processes (collaboration of downward and upward causation). The work demonstrates that such interplay also includes reticulate interactions and reticulate causation. In this regard, we exemplify how community systems provide various non-genetic ‘scaffoldings’, ‘constraints’, and ‘affordances’ for individual and sociocultural evolutionary development. Such research complements prevailing models that focus on the vertical transmission of heritable information, from parent to offspring, with research that instead focusses on horizontal, oblique and even reverse information transmission, going from offspring to parent. We call this reversed information transfer the ‘offspring effect’ to contrast it from the ‘parental effect’. We argue that the proposed approach to inheritance is effective for modelling cumulative and distributed developmental process and for explaining the biological origins and evolution of language. (shrink)

That holobionts are units of selection squares poorly with the observation that microbes are often recruited from the environment, not passed down vertically from parent to offspring, as required for collective reproduction. The taxonomic makeup of a holobiont’s microbial community may vary over its lifetime and differ from that of conspecifics. In contrast, biochemical functions of the microbiota and contributions to host biology are more conserved, with taxonomically variable but functionally similar microbes recurring across generations and hosts. To save what (...) is of interest in holobiont thinking, we propose casting metabolic and developmental interaction patterns, rather than the taxa responsible for them, as units of selection. Such units need not directly reproduce or form parent-offspring lineages: their prior existence has created the conditions under which taxa with the genes necessary to carry out their steps have evolved in large numbers. These taxa or genes will reconstruct the original interaction patterns when favorable conditions occur. Interaction patterns will vary in ways that affect the likelihood of and circumstances under which such reconstruction occurs. Thus, they vary in fitness, and evolution by natural selection will occur at this level. It is on the persistence, reconstruction, and spread of such interaction patterns that students of holobiosis should concentrate, we suggest. This model also addresses other multi-species collectively beneficial interactions, such as biofilms or biogeochemical cycles maintaining all life. (shrink)

It is argued that multiscale approaches are necessary for an explanatory modeling of biological systems. A first step, besides common to the multiscale modeling of physical and living systems, is a bottom-up integration based on the notions of effective parameters and minimal models. Top-down effects can be accounted for in terms of effective constraints and inputs. Biological systems are essentially characterized by an entanglement of bottom-up and top-down influences following from their evolutionary history. A self-consistent multiscale scheme is proposed to (...) capture the ensuing circular causality. Its differences with standard mean-field self-consistent equations and slow-fast decompositions are discussed. As such, this scheme offers a way to unravel the multilevel architecture of living systems and their regulation. Two examples, genome functions and biofilms, are detailed. (shrink)

Organisms possess a special unity that biologists have long recognized and that cries out for explanation. Organs and collectives also have their own related kinds of unity, so what distinguishes the unity of the organism? I argue that only substantial form, a central plank of hylemorphic metaphysics, can provide the explanation we need. I set out the idea that whilst organisms possess substantial form, organs abtain the substantial form of the organisms they belong to, and collectives contain the substantial forms (...) of their organismic members. I consider a number of difficult cases, including lichens, biofilms, cellular slime moulds, and plasmodial slime moulds, arguing that none of them pose a serious threat to the threefold distinction between organ, organism, and collective. I conclude by arguing that two prominent, alternative unity principles for organisms do not work, thus giving indirect support to the need for substantial form. (shrink)

In the 1970s, R.D. MacElroy coined the term ‘extremophile’ to describe microorganisms that thrive under extreme conditions (MacElroy 1974). This hybrid word transliterates to ‘love of extremes’ and has been studied as a straightforward concept for the past 40 years. In this paper, we discuss several ways the term has been understood in the scientific literature, each of which has different consequences for the distribution and importance of extremophiles. They are, briefly, Human-Centric, at the Edge of life’s habitation of Morphospace, (...) by appeal to Statistical Rarity, described by Objective Limits, and at the Limits of Impossibility for metabolic processes. Importantly, these concepts have co-existed, unacknowledged and conflated, for decades. Confusion and equivocation threaten to follow from the wildly varied inclusion or exclusion of organisms as extremophiles depending on the concept used. Under some conceptions, entire kinds of extremophiles become meaningless. Since our understanding of how life works is shaped by what we take to be its extremes, clarifying extremophily is key for many large-scale projects in biology, ecology, biotechnology and astrobiology. In what follows, we proceed as if a noncontroversial account of life is possible and that it is possible to find complex chemistry in the Universe that is similar enough to Life on Earth such that both may be considered instances of ‘life’ (but see Mariscal & Doolittle 2018). We raise, but do not address, the questions of whether the distribution of Life on Earth is representative of what we may find elsewhere in the Universe, whether the same kinds of extremophiles would exist given a replay of the tape of life. Additionally, each of these concepts assumes life based on some sort of biochemistry in this universe, effectively setting aside claims made by some artificial life proponents that their digital organisms are genuine examples of life (Langton 1989, Ray 1995). On the distinction between extremophilic and extremotolerant, we note that all accounts accept the latter as a broader category than the former, since ‘phily’ means love and tolerance is a prerequisite for love under any conception. Indeed, there will be many extremely impoverished environments where tolerance is the only option and thriving is precluded, e.g. Bacillus marismortui was extracted and grown from 250-million-year-old salt crystals in the Permian Salado Formation in an inactive yet persistent state (Vreeland et al., 2000). We also note that extremophily, as a functional category, is potentially applicable at many levels of the biological hierarchy. Extremophily at one level does not necessarily extend to higher and lower levels. For instance, a microorganism in isolation might be quite intolerant to certain environmental conditions yet flourish when subjected to the same conditions as a community or natural biofilm. Alternatively, a protein molecule might be quite stable or active under certain conditions even if the optimal environment for the organism containing it is far more mesophilic. There is an industry of artificially selecting organisms and proteins to adapt to extreme environments (see van den Burg & Eijsink 2002), providing some justification to consider ‘functioning at extremes’ as a worthwhile category of investigation. Finally, we also note certain physico-chemical ranges are rarely considered with respect to extremophily – timespan, size, nutrient availability (Hoehler & Jørgensen 2013), etc. – as well as some biological parameters – abundance, isolation, competition, etc. Perhaps scientific interest must also come into play as to the reason these criteria are not considered relevant. We return to this issue later. In the next section, we give five definitions of extremophily, show their benefits, drawbacks, and unintended yet unavoidable consequences. These arguments are summarized in Table 1 and represented visually in Figures 1 and 2. Given research on polyextremophiles, it seems Figure 2 is a more plausible representation of the state of current knowledge than Figure 1 (Harrison et al. 2013). Life is patchily distributed across various dimensions, which may reflect its contingent history, poor sampling, or (perhaps) fundamental limits. Figure 3 shows the conceptual flowchart for all of these views. In the following section, we take a step back to ask whether we should choose between these definitions and how such a judgment could be made. We argue for a limited pluralism, in which some, but not all, of the concepts are acceptable relative to certain practical and theoretical aims. (shrink)

Individual bacterial cells can communicate via quorum sensing, cooperate to harvest nutrients from their environment, form multicellular biofilms, compete over resources and even kill one another. When the environment that bacteria inhabit is an animal host, these social behaviours mediate virulence. Over the last decade, much attention has focussed on the ecology, evolution and pathology of bacterial cooperation, and the possibility that it could be exploited or destabilised to treat infections. But how far can we really extrapolate from theoretical predictions (...) and laboratory experiments to make inferences about ‘cooperative’ behaviours in hosts and reservoirs? To determine the likely importance and evolution of cooperation ‘in the wild’, several questions must be addressed. A recent paper that reports the dynamics of bacterial cooperation and virulence in a field experiment provides an excellent nucleus for bringing together key empirical and theoretical results which help us to frame – if not completely to answer – these questions. (shrink)

Diverse living systems possess the capacity for regeneration; that is, they can under some circumstances repair, re-produce, and maintain themselves in the face of disturbance or damage. Think of systems as diverse as forests, microbial biofilms, corals, salamanders, hydra, and human skin cells. This capacity is fundamental to life—without it, many biological systems would be too fragile to cope with stress and would frequently collapse—but because it is multiply realized in wildly different living systems at many scales, finding a common (...) understanding may seem futile, and in fact research has proceeded along independent lines. For example, the sciences of organismal regeneration and ecological regeneration appear to have little more than a nominal relationship. Progress towards unification can be made, we think, by turning to evolutionary theory, specifically by synthesizing recent discussions of the evolution of individuals versus collectives with older literature about replicators versus interactors. This allows us to provide a partial answer in response to MacCord and Maienschein’s call for “basic units and mechanisms” of regeneration, relevant when that process is “adaptive.” We argue that the basics of adaptive regeneration can be understood and generalized through a modification of David Hull’s replicator-interactor framework. (shrink)

Extracellular nucleic acids are found in different biological fluids in the organism and in the environment: DNA is a ubiquitous component of the organic matter pool in the soil and in all marine and freshwater habitats. Data from recent studies strongly suggest that extracellular DNA and RNA play important biological roles in microbial communities and in higher organisms. DNA is an important component of bacterial biofilms and is involved in horizontal gene transfer. In recent years, the circulating extracellular nucleic acids (...) were shown to be associated with some diseases. Attempts are being made to develop noninvasive methods of early tumor diagnostics based on analysis of circulating DNA and RNA. Recent observations demonstrated the possibility of nucleic acids exchange between eukaryotic cells and extracellular space suggesting their participation in so far unidentified biological processes. BioEssays 29:654–667, 2007. © 2007 Wiley Periodicals, Inc. (shrink)

The sociobiology of bacteria, largely unappreciated and ignored by the microbiology research community two decades ago is now a major research area, catalyzed to a significant degree by studies of communication and cooperative behavior among the myxobacteria and in quorum sensing (QS) and biofilm formation by pseudomonads and other microbes. Recently, the topic of multicellular cooperative behaviors among bacteria has been increasingly considered in the context of evolutionary biology. Here we discuss the significance of two recent studies1,2 of the (...) phenomenon of “cheating” mutants and their exploitation of cooperating microbial populations of Pseudomonas aeruginosa. BioEssays 30:296–298, 2008. © 2008 Wiley Periodicals, Inc. (shrink)

Nature is replete with borderline cases that fall somewhere between organisms and communities, such as lichens, biofilms, and the Portuguese Man-of-War. At first glance, the existence of such borderline cases might suggest that the concept of what constitutes an organism is too fuzzy to be useful in evolutionary biology. Yet, the notion of organisms is entrenched within central debates in evolution, including discussions over how fitness should be measured, what the bearers of adaptations and fitness are, and the status of (...) holobionts. Finally, accounts of organisms can set the stage for explanations of how multicellularity evolved. In particular, characterizing multicellular organisms in terms of the level of cooperation between their cells suggests that their evolution required the presence of mechanisms that could suppress conflict between cells. (shrink)

Microbes often live in association with dense multicellular aggregates, especially biofilms, and the construction of these aggregates typically requires microbial cells to produce public goods, such as enzymes and signaling molecules. Public-goods producers are, in turn, vulnerable to exploitation by free-rider cells that consume the public goods without paying for their production costs. The cell population of a biofilm or other microbial aggregates are expected to pass through bottlenecks due to a wide range of factors, such as antibiotic treatments (...) and dispersal. The goal of this article is to make the case for the relevance of population bottlenecks at shaping the social interactions within microbial aggregates. The effect of bottlenecks on microbial aggregates is complex in that bottlenecks can favor producers under certain circumstances, but not in others. The concept of the Volunteer’s Dilemma from game theory will be used to motivate the hypothesis that this partly occurs because of how bottlenecks alter the risk of being a producer in a microbial aggregate. Finally, the role of bottlenecks in the microbial world impacts key issues in evolutionary biology, including the importance of ecology at shaping social evolution, and the evolution of multicellularity from unicellular ancestors. (shrink)

Philosophers of biology, along with everyone else, generally perceive life to fall into two broad categories, the microbes and macrobes, and then pay most of their attention to the latter. ‘Macrobe’ is the word we propose for larger life forms, and we use it as part of an argument for microbial equality. We suggest that taking more notice of microbes – the dominant life form on the planet, both now and throughout evolutionary history – will transform some of the philosophy (...) of biology’s standard ideas on ontology, evolution, taxonomy and biodiversity. We set out a number of recent developments in microbiology – including biofilm formation, chemotaxis, quorum sensing and gene transfer – that highlight microbial capacities for cooperation and communication and break down conventional thinking that microbes are solely or primarily single-celled organisms. These insights also bring new perspectives to the levels of selection debate, as well as to discussions of the evolution and nature of multicellularity, and to neo-Darwinian understandings of evolutionary mechanisms. We show how these revisions lead to further complications for microbial classification and the philosophies of systematics and biodiversity. Incorporating microbial insights into the philosophy of biology will challenge many of its assumptions, but also give greater scope and depth to its investigations. (shrink)

Este artículo de revisión examina la importancia que tienen las comunidades microbianas que colonizan los ambien­tes y equipos de procesado de alimentos formando biopelículas o biofilms en la persistencia microbiana en la industria alimen­taria y consecuentemente, en la seguridad y la calidad de los alimentos. La atención se centra especialmente en biopelículas formadas por microorganismos no deseados, es decir, microor­ganismos alterantes y patógenos. Se presenta información so­bre la variabilidad intraespecífica en la formación, la ecología y la arquitectura de las biopelículas, (...) y los factores que influyen en su formación. Asimismo, se resume la información disponible sobre nuevos agentes o estrategias para el control de la forma­ción o eliminación de biopelículas. (shrink)

Chemosensory systems are complex regulatory pathways capable of perceiving external signals and translating them into different cellular behaviors such as motility and development. In the δ-proteobacterium Myxococcus xanthus, chemosensing allows groups of cells to orient themselves and aggregate into specialized multicellular biofilms termed fruiting bodies. M. xanthus contains eight predicted CSS and 21 chemoreceptors. In this work, we systematically deleted genes encoding components of each CSS and chemoreceptors and determined their effects on M. xanthus social behaviors. Then, to understand how (...) the 21 chemoreceptors are distributed among the eight CSS, we examined their phylogenetic distribution, genomic organization and subcellular localization. We found that, in vivo, receptors belonging to the same phylogenetic group colocalize and interact with CSS components of the respective phylogenetic group. Finally, we identified a large chemosensory module formed by three interconnected CSS and multiple chemoreceptors and showed that complex behaviors such as cell group motility and biofilm formation require regulatory apparatus composed of multiple interconnected Che-like systems. © 2014 Moine et al. (shrink)

In Europe ≈15,000 patients receive larval therapy for wound treatment annually. Over the past few years, clinical studies have demonstrated the success of larvae of Lucilia sericata as debridement agents. This is based on a combination of physical and biochemical actions. Laboratory investigations have advanced our understanding of the biochemical mechanisms underlying the beneficial effects of larval secretions, including removal of dead tissue, reduction of the bacterial burden, and promotion of tissue regeneration. The present article summarizes our current understanding of (...) the microbiological, immunological, and wound healing actions of larval therapy, and the molecules involved in these beneficial effects. Future studies will focus on the isolation, identification, and (pre)clinical testing of the effective molecules of L. sericata larvae. These molecules may be candidates for the development of new agents for the treatment of several infectious and inflammatory diseases, including chronic wounds. (shrink)

Staphylococcus aureus is an opportunistic pathogen capable of causing a variety of diseases including osteomyelitis, endocarditis, infections of indwelling devices and wound infections. These infections are often chronic and highly recalcitrant to antibiotic treatment. Persister cells appear to be central to this recalcitrance. A multitude of factors contribute to S. aureus virulence and high levels of treatment failure. These include its ability to colonize the skin and nares of the host, its ability to evade the host immune system and its (...) development of resistance to a variety of antibiotics. Less understood is the phenomenon of persister cells and their role in S. aureus infections and treatment outcome. Persister cells occur as a sub‐population of phenotypic variants that are tolerant to antibiotic treatment. This review examines the importance of persisters in chronic and relapsing S. aureus infections and proposes methods for their eradication. (shrink)