Читать книгу Diatom Gliding Motility - Группа авторов - Страница 13

Anyone who has peered into a microscope and observed the movement of diatoms knows they have witnessed an intriguing example of cellular biology. Unlike most other of their sister algae, this movement involves neither swimming through solution (like Euglena or Chlamydomonas) or amoeboid crawling of membrane and cytoplasm (like Synchroma). Surrounded by a hardened silicified cell wall, motile diatoms are still able to glide gracefully along surfaces while the cell protoplast remains contained within these ornate cell walls. As such, the mysteries involving this curious form of movement have been of interest for well over a hundred years, and models of many sorts have been proposed to explain it (see [1.20]).

Our hope is that this volume will help to not only convey our excitement about research in diatoms, but also demonstrate a variety of techniques and approaches currently used to understand some of the aspects of diatom movement. We have included chapters centering on a number of areas: detailed observation of movements [1.23] [1.43], cellular aspects of motility [1.5] [1.8], ecology and environmental interactions [1.13] [1.40] [1.44], more passive and epiphitic movements [1.18] [1.42], new and novel methodologies [1.2] [1.51] and potential models of motility [1.7] [1.20] [1.47].

Our goal is not to vigorously promote and defend any one particular model, but rather to present the reader with the variety of experimental approaches that are currently being used to address the problem. In this way readers will be able to assess for themselves the areas of diatom motility that require further exploration, and the predictions of various models that still need to be tested. For example, the exact mechanism of force production for diatom motility is still unresolved. While models of force generation arising from motor proteins interacting with the cytoskeleton and coupled to secreted mucilage strands are favored by some, others currently favor models generating motile force generated by the explosive release and hydration of mucilage regulated by the localization of the secretory site directed by the underlying cytoskeleton.

There are certainly areas of diatom motility that were unfortunately not able to be included in this volume, and we encourage readers to explore these areas if they wish to be more fully aware of important work in the field. In particular, the editors want to note a number of areas of diatom motility that are not fully addressed in the current volume or are open areas and questions needing more research:

Chemotaxis: Understanding the chemical triggers that can stimulate and help regulate diatom movement, especially during cell pairing during reproduction, is crucial to a full understanding of the process. Important work on diatom chemoattractants and pheromones has been done in recent years (e.g., diatom pheromones [1.19] [1.39]), although the mechanisms by which these chemical stimulants interact with and help to regulate the motility generating process are still poorly understood.

Tube-dwelling diatoms: A number of species have the ability to specialize their extracellular secretions to provide their own surfaces for movement [1.27] [1.48], generating types of stalks and tubes through which the diatoms can move, but providing three-dimensional structures important for attachment and ecology of other organisms [1.17] [1.28].

Centric diatoms: While centric diatoms have little or no direct substratum motility as seen with many of the pennate diatoms, they can modify their position in the water column [1.36] and there has been some great recent work demonstrating there is direct regulation of diatom buoyancy [1.16] [1.34]. We encourage readers to explore this topic as well if they wish to be further engaged in current approaches regarding functional regulation of centric movement.

Composition of diatom mucilage: Understanding the chemical and physical nature of diatom mucilages and secretions is important to understanding the way that diatoms can use mucilage for a variety of functions. It is likely that different materials are secreted for purposes such as protection of cells during reproduction, and holding the two halves of their frustule together, stalk production, as well as making connections that can move their position relative to the frustule. A number of prior investigations have begun to look into this (e.g., [1.26] [1.27]) and it seems like a great opportunity for continued future work. It has practical impact in the study of biofouling [1.50] and underwater adhesives.

Photoreception: A number of labs have begun to investigate the types of molecules responsible for photoreception in algae. While numerous types of promising candidates have been described (e.g. [1.12] [1.29] [1.31] [1.35] [1.37]), there have been no definitive studies pointing to specific molecules driving the diurnal, light aggregation, or light avoidance behaviors. Better knowledge of the specific light and chemical receptors in diatoms, and how they alter the processes of force generation and directional bias in cells will be needed too. Light piping in the colonial pennate diatom Bacillaria has been postulated [1.21], but not yet tested.

Effect of morphogenetic alterations on motility: Numerous diatom species have alternative morphologies based on the environmental conditions (e.g., [1.9] [1.30]). In addition, while numerous pennate diatoms are basically symmetric about the transapical plane dividing the two raphe branches (e.g., Navicula spp.), there are also numerous other species (e.g., Gomphonema spp.) in which the raphe runs down the apical axis, but the morphology at the two ends is decidedly different. There are also species where the raphe is displaced along valvar wings and the break between branches is at one end (e.g., Surirella spp.). The characterization of such species, correlating the valve morphology and raphe morphology with motility characteristics, seems like a productive line of research to better determine the relationship between wall structure and movement, and whether the motility associated with the ends of raphe branches can be regulated independently.

Cytoskeletal organization: The actin cables comprised of large bundles of actin filaments underlying the raphe in motile raphid diatoms appear essential to active, well-regulated motility [1.41]. But the connection between the filaments of the cables and the raphe mucilage fibers remains poorly understood. More research definitely needs to be done on more detailed organization of the actin filaments within the larger ultrastructure and orientation of the cell and frustule. The polarity of the two actin cables (parallel? antiparallel?) and relative placement to the membrane are crucial details to resolve.

Evolutionary relationships of motility: While diatom gliding is a somewhat unique form of motility, a clearer understanding of the movement would also arise from a better knowledge of its evolutionary basis. For example, some algae such as desmids or filamentous bacteria can move via direct mucilage secretion through specialized pores [1.10] [1.14] [1.15], some algae like Chara use membrane-associated actin cables to generate intracellular movement and cytoplasmic streaming [1.25] [1.46], and in some cases algae that normally swim (e.g., Chlamydomonas) can glide over a surface using the membranous intracellular transport powered by motor proteins using the underlying cytoskeleton [1.45]. Gliding in myxobacteria [1.49] is similar to that of diatoms. Studying how some of these types of components might be related to diatom gliding could yield important insights into both the evolution and physiology of these types of movements.

In addition to these, there are numerous areas that are ripe for fresh research. Diatom species are a foundational food component to many aquatic ecosystems, and are quite sensitive (in motility, metabolism and reproduction) to temperature fluctuations. Thus, detailed ecological studies of effects of diatoms in changing temperatures would be crucially important to understand the ecological impact of diatoms related to temperature change, daily and long-term. We know that mucilage strength and resilience, and subsequent motile abilities, are all related to temperature and could be severely affected by small temperature changes. Knowing how these motility and adhesion attributes change, and which species are more sensitive, would be a great boost to understanding the ecological ramifications of climate change. Another interesting topic not fully resolved and of interest is determining how expensive such motility really is for the diatoms, as they leave large amounts of extruded carbohydrate externally to the frustule and need to constantly synthesize materials associated with motility. While such mucilage also becomes connected to other ecological issues with a tight-knit algal community, the energy costs for an individual cell is an intriguing question.

Diatom secretions are also strongly related to many ecological structures of aquatic ecosystems [1.4]. They affect soil and sediment stability, food access during diurnal movements, food accessibility in stalked versus benthic forms, and connection and stability within complex algal communities where diatoms can work to interconnect various forms of algae. It would be worthwhile to investigate the details of the mucilage from various forms and species of diatoms in different communities (and, as above, their changes as a function of temperature) in an attempt to understand which secretions (e.g., motility related versus non-motility related) are most important for different aspects of an algal community. Investigating the changes in these secretions, and in the resulting motile characteristics of the cells, will provide a much stronger understanding of the ways diatoms are functionally integrated within an algal community. Moreover, understanding the energetics of motility is crucial to understanding the constraints placed on a cell in its generation of movement. While a recent work has begun to consider the energetics of diatom movement during diurnal migration [1.38], there is much work to be done in understanding the energy consumed by diatoms under different ecological situations.

There is also a strong need for additional work into high resolution forms of microscopy to determine, in living cells, where mucilage is being secreted, the characteristics of the mucilage secreted from the raphe, and the way in which raphe connections to the substratum are correlated with stimuli (e.g., light irradiation) affecting the direction and motility. Understanding the molecular controls on motility within the cell needs additional research to identify the receptors and molecules responsible for regulation and synthesis of the different enzymes and substances needed in the motile machinery.

Despite these many open areas of diatom research into motility, it is also important to reiterate what we do know about diatom motility:

Adhesion and motility are closely coupled: The requirement for raphe secreted mucilage to adhere to a solid or semi-solid substratum in order to move is well supported. Diatom secretions are crucial for a number of cell processes, including protection of protoplasts during cell conjugation, attachment and integrity of cell wall components, formation of stalks, and motility of cells. Inhibitors of diatom secretion inhibit motility, and diatom motility is strongly correlated with the degree to which it can adhere to a substratum. In some research, it has been shown that diatoms on the underside of a surface can also pull themselves back up to a motile confirmation after briefly remaining adhered by only a single end of the cell.

Motile characteristics are species specific: Numerous lines of research have shown that path curvature, mean path lengths, light wavelength stimuli, speed, and strength of adhesion during motility during movement are all species specific. In this way, species determination can be made by distinct characteristics of motile behavior, in addition to more typically used aspects such as frustule ornamentation and detail and life history. Thus, diatoms, like most other organisms, are not just a set of morpho-species separated by evolutionary diversification of frustule design, but have clear physiological differences that relate not just to reproductive ability, but also to everyday photo- and chemo-responsive behaviors.

Motile characteristics of cells are crucial components of local ecology: Every aspect of diatom motility is directly connected to aspects of local aquatic ecology. The amount of secretion has direct effect on sediment stability, rates and sensitivities of photoresponses directly affect diurnal rhythms through sediment and thereby access of diatoms to higher level consumers, movement and mucilage secretion can provide surface conditioning of rocks and surfaces for immigration and colonization of other organisms, differential motile responses can lead to niche partitioning and increased species diversity, and movement of diatoms via epiphytic attachment can drive influx and retention of other species.

Motile characteristics are sensitive to physical and biological ecological conditions: Many studies have shown that pH, ionic composition, temperature, and surface conditions all play a role in motile characteristics of diatom cells. This not only allows surveys of species distributions to help determine the ecological conditions present in various ecosystems, but helps to understand geographical distributions and immigration/emigration characteristics. Moreover, motile characteristics can also be modulated by the presence or absence of other organisms or diatoms, leading to increased movements into areas that allow for lower competition and increased ecological success.

Motility in mudflats along coasts have been studied in detail: Common diatoms in those habitats like Cylindrotheca closterium (Ehrenberg) Reimann & J.C. Lewin have been shown to have four types of movement modalities: gliding (smooth or corkscrew), non-gliding (pivots and rollover), gliding pirouettes and detaching movements [1.3]. Considering the cohesive nature of the mudflat sediment [1.6], corkscrew gliding was reported to help with mechanisms for movement through the fine layers. Responses to salinity included non-gliding movements like rollover and detachment (probably associated with polysaccharide synthesis) [1.1]. Changes in the chemical gradients with the mudflats stimulates pirouettes and pivot movements, helping the cells to escape unfavorable conditions [1.24].

Actin filaments underlying the raphe are crucial to raphid pennate motility: While the way in which the actin filaments contribute to motility is still not fully understood, it is clear that inhibition of actin coordinately inhibits motility. While possibly used for mucilage placement, orientation, or coupling to motor protein force generation, actin importance is undeniable.

Localizations of diatoms during movement is due to directional bias: While many other types of algae and protists can maneuver in elaborate two-dimensional or three-dimensional movements, diatoms mainly are constrained locally to a one-dimensional axis defined by the raphe. Within that local area, movement is essentially regulated by biasing the cell in the direction of movement along that axis. For example, while the intensity and wavelength vary by species, virtually all motile diatoms are biased along the axis to move away from very high irradiance light, and towards more moderate light levels. Similarly, cells triggered to undergo reproduction tend to find other cells to pair with by biased forward/back movements along with random rotations, rather than any kind of true directional reorientation.

Questions raised 20-30 years ago, like whether migration rhythms of sigmoid and nitzschioid biraphid diatoms responding to different stimuli like tides or light [1.22] [1.33] or chemical motility inhibitors working through changes is photosynthetic activity or not [1.11], have been partially answered. The rhythms of diatom movements appear synchronous with tides for large motile representatives of genera like Pleurosigma, Gyrosigma and Navicula. At low tide, movement and speed on the surface of the sediment was observed, ensuring the cells good access to light. At high tide, movement was minimal, probably due to sheer pressure of the water layer above the sediment, making it impossible for microbes to move. Individuals within a colony of Bacillaria paxillifera (O.F. Müller) T. Marsson followed diurnal rhythms and moved only when light was available [1.32]. Chemicals inhibiting myosin-based motility in animals or actin-binding chemical from marine sponges were shown to inhibit diatom motility [1.11] [1.41].

We would like to thank all the authors and contributors to this volume for bringing their joy of diatoms to share with the readers. We hope that this volume will help reinforce the enthusiasm of all those interested in diatom motility, and help them in the search for better understanding of a truly fascinating phenomenon.

The editors would also like to thank all the authors for sharing their knowledge and ideas on diatom motility and for their patience in the process. Also, the editors would like to gratefully acknowledge our external reviewers for agreeing to critique the initial drafts of these manuscripts. These reviewers include: Małgorzata Bąk, Karen Bondoc, Manfred Drack, Natalie Hicks, Kai Lu, James Nienow, Chris Peterson, Tom Portegys, Nicole Poulsen, and Johannes Srajer. Their work has contributed immensely to the quality of the manuscripts.

Stanley A. Cohn Kalina M. Manoylov

Richard Gordon

June 2021