Algae-bacteria interactions: Evolution, ecology and emerging applications.

SUMMARY Biotic and abiotic surfaces in marine waters are rapidly colonized by microorganisms. Surface colonization and subsequent biofilm formation and development provide numerous advantages to these organisms and support critical ecological and biogeochemical functions in the changing marine environment. Microbial surface association also contributes to deleterious effects such as biofouling, biocorrosion, and the persistence and transmission of harmful or pathogenic microorganisms and their genetic determinants. The processes and mechanisms of colonization as well as key players among the surface-associated microbiota have been studied for several decades. Accumulating evidence indicates that specific cell-surface, cell-cell, and interpopulation interactions shape the composition, structure, spatiotemporal dynamics, and functions of surface-associated microbial communities. Several key microbial processes and mechanisms, including (i) surface, population, and community sensing and signaling, (ii) intraspecies and interspecies communication and interaction, and (iii) the regulatory balance between cooperation and competition, have been identified as critical for the microbial surface association lifestyle. In this review, recent progress in the study of marine microbial surface colonization and biofilm development is synthesized and discussed. Major gaps in our knowledge remain. We pose questions for targeted investigation of surface-specific community-level microbial features, answers to which would advance our understanding of surface-associated microbial community ecology and the biogeochemical functions of these communities at levels from molecular mechanistic details through systems biological integration.

Microbial Surface Colonization and Biofilm Development in Marine Environments

The interaction of bacteria with surfaces has important implications in a range of areas, including bioenergy, biofouling, biofilm formation, and the infection of plants and animals. Many of the interactions of bacteria with surfaces produce changes in the expression of genes that influence cell morphology and behavior, including genes essential for motility and surface attachment. Despite the attention that these phenotypes have garnered, the bacterial systems used for sensing and responding to surfaces are still not well understood. An understanding of these mechanisms will guide the development of new classes of materials that inhibit and promote cell growth, and complement studies of the physiology of bacteria in contact with surfaces. Recent studies from a range of fields in science and engineering are poised to guide future investigations in this area. This review summarizes recent studies on bacteria–surface interactions, discusses mechanisms of surface sensing and consequences of cell attachment, provides an overview of surfaces that have been used in bacterial studies, and highlights unanswered questions in this field.

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Bacteria-surface interactions.

The Mechanical World of Bacteria

Adhesion of microbes, such as bacteria and fungi, to surfaces and the subsequent formation of biofilms cause multidrug-tolerant infections in humans and fouling of medical devices. To address these challenges, it is important to understand how material properties affect microbe-surface interactions and engineer better nonfouling materials. Here we review the recent progresses in this field and discuss the main challenges and opportunities. In particular, we focus on bacterial biofilms and review the effects of surface energy, charge, topography, and stiffness of substratum material on bacterial adhesion. We summarize how these surface properties influence oral biofilm formation, and we discuss the important findings from nondental systems that have potential applications in dental medicine.

Effects of Material Properties on Bacterial Adhesion and Biofilm Formation

Biofilms, flagella, and mechanosensing of surfaces by bacteria

Silicibacter sp strain TM1040, a member of the Roseobacter clade, forms a symbiosis with unicellular phytoplankton, which is inextricably linked to the biphasic "swim or stick" lifestyle of the bacteria Mutations in flaC bias the population toward the motile phase Renewed examination of the FlaC(-) strain (HG1016) uncovered that it is composed of two different cells: a pigmented type, PS01, and a nonpigmented cell, PS02, each of which has an identical mutation in flaC While monocultures of PS01 and PS02 had few motile cells (06 and 6%, respectively), coculturing the two strains resulted in a 10-fold increase in the number of motile cells Cell-free supernatants from coculture or wild-type cells were fully capable of restoring motility to PS01 and PS02, which was due to increased fliC3 (flagellin) transcription, FliC3 protein levels per cell, and flagella synthesis The motility-inducing compound has an estimated mass of 226 Da, as determined by mass spectrometry, and is referred to as Roseobacter Motility Inducer (RMI) Mutations affecting genes involved in phenyl acetic acid synthesis significantly reduced RMI, while defects in tropodithietic acid (TDA) synthesis had marginal or no effect on RMI RMI biosynthesis is induced by p-coumaric acid, a product of algal lignin degradation When added to algal cultures, RMI caused loss of motility, cell enlargement, and vacuolization in the algal cells RMI is a new member of the roseobacticide family of troponoid compounds whose activities affect roseobacters, by shifting their population toward motility, as well as their phytoplankton hosts, through an algicidal effect

A Novel Inducer of Roseobacter Motility Is Also a Disruptor of Algal Symbiosis

Proteus mirabilis is a dimorphic, motile bacterium often associated with urinary tract infections. Colonization of urinary tract surfaces is aided by swarmer cell differentiation, which is initiated by inhibition of flagellar rotation when the bacteria first contact a surface. Mutations in fliL, encoding a flagellar structural protein with an enigmatic function, result in the inappropriate production of differentiated swarmer cells, called pseudoswarmer cells, under noninducing conditions, indicating involvement of FliL in the surface sensing pathway. In the present study, we compared the fliL transcriptome with that of wild-type swarmer cells and showed that nearly all genes associated with motility (flagellar class II and III genes) and chemotaxis are repressed. In contrast, spontaneous motile revertants of fliL cells that regained motility yet produced differentiated swarmer cells under noninducing conditions transcribed flagellar class II promoters at consistent levels. Expression of umoA (a known regulator of swarmer cells), flgF, and flgI increased significantly in both swarmer and pseudoswarmer cells, as did genes in a degenerate prophage region situated immediately adjacent to the Rcs phosphorelay system. Unlike swarmer cells, pseudoswarmers displayed increased activity, rather than transcription, of the flagellar master regulatory protein, FlhD4C2, and analyses of the fliL parent strain and its motile revertants showed that they result from mutations altering the C-terminal 14 amino acids of FliL. Collectively, the data suggest a functional role for the C terminus of FliL in surface sensing and implicate UmoA as part of the signal relay leading to the master flagellar regulator FlhD4C2, which ultimately controls swarmer cell differentiation.

Perturbation of FliL interferes with Proteus mirabilis swarmer cell gene expression and differentiation.

Proteus mirabilis is a dimorphic motile bacterium well known for its flagellum-dependent swarming motility over surfaces. In liquid, P. mirabilis cells are 1.5- to 2.0-μm swimmer cells with 4 to 6 flagella. When P. mirabilis encounters a solid surface, where flagellar rotation is limited, swimmer cells differentiate into elongated (10- to 80-μm), highly flagellated swarmer cells. In order for P. mirabilis to swarm, it first needs to detect a surface. The ubiquitous but functionally enigmatic flagellar basal body protein FliL is involved in P. mirabilis surface sensing. Previous studies have suggested that FliL is essential for swarming through its involvement in viscosity-dependent monitoring of flagellar rotation. In this study, we constructed and characterized ΔfliL mutants of P. mirabilis and Escherichia coli. Unexpectedly and unlike other fliL mutants, both P. mirabilis and E. coli ΔfliL cells swarm (Swr+). Further analysis revealed that P. mirabilis ΔfliL cells also exhibit an alteration in their ability to sense a surface: e.g., ΔfliL P. mirabilis cells swarm precociously over surfaces with low viscosity that normally impede wild-type swarming. Precocious swarming is due to an increase in the number of elongated swarmer cells in the population. Loss of fliL also results in an inhibition of swarming at <30°C. E. coli ΔfliL cells also exhibit temperature-sensitive swarming. These results suggest an involvement of FliL in the energetics and function of the flagellar motor.

Loss of FliL Alters Proteus mirabilis Surface Sensing and Temperature-Dependent Swarming

Summary
Bacteria live either as independent planktonic cells or as members of surface-attached communities called biofilms. Motility and biofilm development are mutually exclusive events, and control of the phase of this ‘swim-or-stick’ switch involves the ability of the bacterium to sense and respond appropriately to a surface. Cairns et al. (2013) report that the Bacillus subtilis flagellum functions in surface-sensing. Using mutants of B. subtilis that prevent flagellum rotation, they measured the expression and activity of DegU, the response regulator of the two-component DegS–DegU circuit. DegU activity and degU transcription increased when flagellum rotation was prevented, and were dependent on the DegS kinase. Inhibiting flagellar rotation by overexpressing the EpsE flagellar ‘clutch’ or addition of anti-flagellin antiserum also increased degU transcription and activity. These results suggest B. subtilis senses restriction of flagellum rotation as the cell nears a surface. Inhibition of the flagellum activates the DegS–DegU circuit to turn on biofilm formation, i.e. the flagellum is acting as a mechanosensor of surfaces. B. subtilis joins an ever-expanding group of bacteria, including species of Vibrio, Proteus and Caulobacter that use the flagellum as a surface sensor.

Robert Belas

Papers

Biofilms, flagella, and mechanosensing of surfaces by bacteria

A Novel Inducer of Roseobacter Motility Is Also a Disruptor of Algal Symbiosis

Perturbation of FliL interferes with Proteus mirabilis swarmer cell gene expression and differentiation.

Loss of FliL Alters Proteus mirabilis Surface Sensing and Temperature-Dependent Swarming

When the swimming gets tough, the tough form a biofilm