Abstract
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.
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Notes
Other collective associations of prokaryotes include colonies stemming from the clones of single species bacteria/archaea (e.g. Lactococcus lactis or Streptococcus thermophilus) or intracellular parasites (e.g. Vampirococcus and Bdellovibrio). We will not analyse these cases here as they do not exhibit the features of a stable functionally integrated collective organisation. In the first case, they do not exhibit a common spatial constraint, the EPS matrix. In the second case intracellular parasitism is a transient not functionally integrated relationship where the host is killed.
The focus on current forms of endosymbiosis as a possible way to provide valuable clues as to the role played by endosymbiosis in the achievement of a ‘strong’ physiological integration in eukaryogenesis moves in a similar direction to the one explored by Reyes-Prieto et al. (2014). They focus on non-autonomous endosymbionts with extremely reduced genomes, or ‘symbionelles’, to shed light on the origin of eukaryotic organelles.
This idea is in line with the thesis that all multicellular association need to solve the issue of spatial control, and that different ways of doing so result in different types of organisations and different degrees of integration (Bich et al. 2019).
Although the term ‘prokaryote’ is nowadays substituted by Bacteria and Archaea, for the sake of simplicity we continue to employ this word in the paper to intend the unicellular organisms belonging to the two domains of Bacteria and Archaea.
As pointed out by Catania et al. (2017), regulatory networks play a pivotal role in defining the functional integration of symbiotic partners. These interdependent networks may be co-inherited (via vertical gene transfer) or re-established in a new generation (via horizontal gene transfer). This argument is also in line with Bich et al. (2016), who have argued that a functionally integrated organisation hinges on a complex set of regulatory mechanisms that allow it to coordinate the contributions of its functional parts and to handle perturbations.
Adhesins are cell-surface structures of bacteria that mediate transient or permanent surface attachment.
Short range control relies on local cell-to-cell direct interactions. Medium range control is achieved when an ensemble of cells is constrained for example by the ECM. In multicellular organisms such as animals it happens at the level of tissues. QS relies on signals and it can be considered as a distributed medium range control mechanism because it can affect a large number of cells by generating self-organised gradients. Long range control, instead, has a systemic reach and has the potential to constrain the activity of all the parts of the system. An example of long-range control mechanisms from animals is the release of hormones, distributed throughout the system through vascularization (see Bich et al. 2019 for more details).
Let us consider, for example, the colonisation of the human oral cavity by the bacterial species Veillonella atypica and Streptococcus gordonii. In order to colonise dental surfaces, V. atypica requires the presence of S. gordonii, because S. gordonii ferments sugars and releases lactic acid, which constitutes the preferred carbon source for V. atypica. The co-aggregation of bacteria from the two species is made possible by the fact that V. atypica produces a soluble chemical signal that triggers amylase expression in S. gordonii, thereby increasing the degradation of complex carbohydrates and lactic-acid production (Keller and Surette 2006).
By ʻco-metabolismʼ, we mean the simultaneous degradation of two compounds: the degradation of the second compound hinges on the presence of the first compound.
By ʻsyntrophyʼ, we refer to the phenomenon by which one species feeds on the by-products of another species.
For example, it lacks collagen IV, which promotes the realisation of interfaces and organ formation in eukaryotic multicellular systems, due to the role it plays in the basement membranes (Fidler et al. 2017).
By ʻevolutionary stable relationshipʼ, we mean a relationship that persist across several generations and that undergoes natural selection as a whole.
Intracellular bacteria have been identified in some blue-green algae of the species Pleurocapsa minor in the seventies (Wujek 1979), but the physiology of this association has not been investigated. Other cases of intracellular bacteria invading the periplasm (e.g. Bdellovibrio) or the cytoplasm (e.g. Daptobacter) of other bacteria have been found (Corsaro and Venditti 2006). However, these cases represent transient symbiotic relationships (i.e. parasites) that do not give rise to an evolutionary stable relationship.
For the sake of our argument, we just focus on the endosymbiotic relationship between the two bacteria (Tremblaya and Moranella), leaving aside the functional contribution of the insect. Indeed, this paper studies the functional integration of associations of prokaryotes and not the functional interdependence between prokaryotes and (multicellular) eukaryotes. Therefore, for clarity, hereinafter we will use the term ʻhostʼ to refer to Tremblaya, whereas the term ʻendosymbiontʼ refers to Moranella. We will use “mealybug cells” for those eukaryotic cells that contain the Tremblaya-Moranella association.
Tremblaya’s genome is 138,927 bp in length, whereas Moranella’s is 538, 924 bp (McCutcheon and von Dohlen 2011). The difference in genome size between Tremblaya and Moranella is consistent with the hypothesis that Moranella penetrated Tremblaya as a secondary endosymbiotic event (López-Madrigal et al. 2013a).
The [Fe-S]-cluster is a prosthetic group mainly involved in oxidation–reduction reactions. It plays several important functions related to energy metabolism and regulation. In particular, it plays a role in bacterial (and mitochondrial) respiratory complexes, in enzyme catalysis and in the sensing environmental or intracellular conditions to regulate gene expression (Lill 2009).
See López-Madrigal et al. (2013a) for the details.
By ‘functional complementation’, we mean the exchange of components that perform, or contribute to, specific functions (such as proteins, tRNA, parts of ribosomal machinery etc.) between the members of the association. It is different from ‘metabolic complementation’ which, instead, consists in the exchange of intermediate metabolic substrates.
The same happens, in lesser degree, in the opposite direction from Tremblaya to Moranella.
Exchanging small molecules such as amino acids and metabolites is deeply different than exchanging proteins, tRNA or other big molecules, and the two cases depend on distinct mechanisms of transport. Unlike our case study, the endosymbiotic relationship between an eukaryotic host and prokaryotic endosymbionts usually relies only on the exchange of amino acids between the two partners. The import of amino acids into the endosymbionts and the export of other amino acids to the host is usually mediated by transporters provided by the host (Duncan et al. 2014).
A translocon is a complex of secretory (ʻsecʼ) proteins involved in the translocation of polypeptides across the membranes.
Osmotic stress (or shock) is a sudden change in the solute concentration around a cell causing a change in the movement of water across the cell membrane.
The loss of genes is an interesting feature of many commensal and mutualistic (symbiotic) relationships and it has been hypothesised that it increases the fitness of the overall associations. Morris et al. (2012) have coined the expression of “Black Queen hypothesis” to posit that “certain genes or, more broadly, biological functions, are analogous to the queen of spades. Such functions are costly and therefore undesirable, leading to a selective advantage for organisms that stop performing them. At the same time, the function must provide an indispensable public good, necessitating its retention by at least a subset of the individuals in the community (Morris et al. 2012). In most cases what is shared is metabolic products, giving rise to forms of ‘syntrophic integration’ by forming ecological networks (Skillings, 2019). In other cases the members of the association share functional components (under collective constraints such as EPS matrix or a common boundary), thus giving rise to forms of cross-control allowing for forms of ‘physiological integration’ (Bich, 2019).
By ‘cross-control’, we mean one partner producing the components that control processes in the other.
By ‘interlocked’ regulation, we mean the activity of regulatory mechanisms which rely on the components produced by both partners.
The Moranella-Tremblaya consortium realises transport through a very basic mechanism based on osmosis in presence of a weakened membrane. In spite of being unspecific and inefficient, it can guarantee the viability of the consortium in the very stable environment of mealybug cells. In fact, this particular mechanism lacks complex channels and mechanisms for protein targeting that would allow much more specific control upon the localisation of functional components. A more stable and robust solution to this problem would instead require a much deeper re-organisation of the systems involved, which is indeed what it is supposed to have happened during the process of eukaryogenesis.
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Funding
This study was funded by the Basque Government (Project: IT1228-19), Ministerio de Ciencia, Innovación y Universidades, Spain (research project PID2019-104576GB-I00 for GM, LB and AM, and ‘Ramon y Cajal’ Programme RYC-2016-19798 for LB), University of the Basque Country (UPV/EHU), Spain (predoctoral scholarship PIF17/31 for GM).
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Militello, G., Bich, L. & Moreno, A. Functional Integration and Individuality in Prokaryotic Collective Organisations. Acta Biotheor 69, 391–415 (2021). https://doi.org/10.1007/s10441-020-09390-z
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DOI: https://doi.org/10.1007/s10441-020-09390-z