Gliding toward new discoveries in diatom adhesion and motility

Pennate diatoms often dominate the photosynthetic microbial communities that support the healthy functioning of shallow soft-sediment ecosystems (Hope et al. 2020). Motility is a key adaptation that has enabled the success of these organisms at the water–substrate interface, where conditions can be extreme and subject to regular fluctuations (Nakov et al. 2018, Hope et al. 2020). The ability to navigate within the sediment is essential to avoid desiccation, locate optimal light and nutrient conditions, and to find a mate for sexual reproduction (Poulsen et al. 2023). In addition, vertical diatom migrations can serve important ecosystem functions by contributing to nutrient cycling between the surface and the subsurface (Merz et al. 2021). The unique ability to adhere to underwater surfaces is also of practical interest. Diatoms are major components of microbial biofilms that develop on submerged surfaces (Molino and Wetherbee 2008), which can reduce mechanical function of equipment or increase drag on a vessel, incurring higher fuel costs. Understanding the mechanisms underlying the diatom adhesive material could inspire the development of new anti-fouling materials that are resistant to diatom colonization. In addition, the chemical properties of the adhesive may also be of interest to develop novel bonding agents that are able to function underwater. The gliding motion observed in diatoms is unique among microbial eukaryotes, as it does not involve swimming, use of additional appendages, or alteration of cell shape (Poulsen et al. 2022). Instead, the force for the gliding mechanism is hypothesized to be driven by an actin-myosin based system (Edgar and Pickett-Heaps 1984, Wetherbee et al. 1998). In this model, adhesive mucilage is secreted from the longitudinal slit in the frustule, termed the raphe, and interacts with an intracellular actin–myosin motor via transmembrane proteins to provide the traction needed for cell movement (Poulsen et al. 2023). While the role of actin and myosin in this mechanism has been supported by drug inhibition studies (Poulsen et al. 1999), the identity of the other proteins in the adhesion–motility complex, including the transmembrane proteins and the proteins in the adhesive mucilage, remain largely unknown. In this issue of the Journal of Phycology, Poulsen et al. (2023) lay the foundation to establish the pennate diatom Craspedostauros australis as a model species for studying diatom adhesion and motility. While C. australis is a highly motile diatom (unlike Phaeodactylum tricornutum, which has historically been a favored species for diatom molecular studies), the lack of a genetic toolkit has previously hindered the utility of C. australis as a model system. To advance the genetic and molecular resources available for C. australis, the authors generated a genome assembly and a transcriptomic dataset that captures gene expression during active gliding. These sequence data will be essential to identifying novel proteins putatively involved in the motility mechanism. Additionally, a particle bombardment-based genetic transformation system was developed, making protein localization and functional genetic studies accessible in this species. The authors leverage these new genetic tools to further investigate frustule-associated components (FACs) thought to be involved in the pennate diatom adhesion–motility complex. FACs isolated from Craspedostauros australis frustules were determined to be isoforms of the same protein, derived from a 3478 bp long gene termed Craspedostauros australis Frustule Associated Protein 1 (CaFAP1). The predicted protein is most similar to mucin-like glycoproteins that share a characteristic structure of alternating proline- and serine/threonine-rich domains and cysteine-rich domains (Fig. 1a). Beyond these domains, however, the sequence of CaFAP1 appears to be unique to C. australis. The presence of CaFAP1 was confirmed in the cell wall and to diatom adhesive trails by both immunofluorescence and fluorescent tagging with GFP, but the proteins are surprisingly absent from the raphe slit and the center of the adhesive trails (Fig. 1, b–d), suggesting that they may be deposited onto the trails as the silica ribs that border the raphe come into contact with the surface. This information, coupled with the fact that limited differences were detected in adhesion strength and gliding velocity between wild-type and CaFAP1-GFP expressing mutants, exclude CaFAP1 from being directly involved with generating the force or traction required for gliding. However, the localization of CaFAP1 and similarity to other mucin-like proteins potentially suggests a functional role in lubrication and self-cleaning. Due to their biomineralized cell walls, diatoms have evolved innovative ways of interacting with and adapting to their environment. In the case of benthic pennate diatoms, the ability of gliding has enabled them to overcome the challenges of movement without change in cell shape, and has provided advantages that have allowed them to expand into diverse habitats. The unique biology of diatoms makes the study of these organisms both fascinating and difficult; diatom cell wall-associated proteins, in particular, often have unknown functions and low homology to annotated proteins in other organisms. However, the authors in this study have demonstrated the careful research necessary to begin to illuminate the function of these novel and interesting cell wall proteins. While some components of the adhesive–motility remain elusive, Poulsen and co-authors have established a model system that is better suited to answer some of the most pressing questions related to diatom motility, setting the stage for new discoveries of both ecological and technological interest.