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50 I. 50 II. 52 III. 53 IV. 66 V. 71 VI. 72 VII. 74 75 References 75 SUMMARY: Cryptospores, recovered from Ordovician through Devonian rocks, differ from trilete spores in possessing distinctive configurations (i.e. hilate monads, dyads, and permanent tetrads). Their affinities are contentious, but knowledge of their relationships is essential to understanding the nature of the earliest land flora. This review brings together evidence about the source plants, mostly obtained from spores extracted from minute, fragmented, yet exceptionally anatomically preserved fossils. We coin the term ‘cryptophytes’ for plants that produced the cryptospores and show them to have been simple terrestrial organisms of short stature (i.e. millimetres high). Two lineages are currently recognized. Partitatheca shows a combination of characters (e.g. spo‐rophyte bifurcation, stomata, and dyads) unknown in plants today. Lenticulatheca encompasses discoidal sporangia containing monads formed from dyads with ultrastructure closer to that of higher plants, as exemplified by Cooksonia. Other emerging groupings are less well characterized, and their precise affinities to living clades remain unclear. Some may be stem group embryophytes or tracheophytes. Others are more closely related to the bryophytes, but they are not bryophytes as defined by extant representatives. Cryptophytes encompass a pool of diversity from which modern bryophytes and vascular plants emerged, but were competitively replaced by early tracheophytes. Sporogenesis always produced either dyads or tetrads, indicating strict genetic control. The long‐held consensus that tetrads were the archetypal condition in land plants is challenged.

Programmed Cell Death (PCD) in eukaryotes is a regulated process occurring during development, cell differentiation and aging. Apoptosis is a particularly well studied morphotype of PCD, only observed in animal cells (metazoan). Its most definitive hallmark is the formation and release of membrane-enclosed extracellular vesicles called Apoptotic Bodies (ABs). Although apoptotic-like features have been described in plants, yeast, protozoa and phytoplankton, the production of ABs has been thought to be limited to multicellular animals. Here we report the production and release of extracellular ABs in a non-metazoan unicellular eukaryote, the cryptophyte alga Guillardia theta . Morphologies of G. theta cells during aging and pharmacologically-induced cell death confirm the presence of ABs and apoptosis in phytoplankton. G. theta ABs have similar composition to metazoan ABs, carrying DNA, proteins, lipids, carbohydrates, fragments of organelles and cytosol portions. Our results demonstrate that G. theta , a microalga that arose from secondary endosymbiosis, experiences apoptotic cell death in physiological conditions, similar to animal cells. Since secondary endosymbiosis occurred prior to the origin of multicellularity, our discovery questions the evolutionary origin of PCD. Here the authors show that a single-celled, photosynthetic alga produces apoptotic bodies during programmed cell death. This mechanism, which was thought to be unique to animals, seems to be more ancient and widespread than previously believed.

An important missing piece in the puzzle of how plastids spread across the eukaryotic tree of life is a robust evolutionary framework for the host lineages. Four assemblages are known to harbour plastids derived from red algae and, according to the controversial chromalveolate hypothesis, these all share a common ancestry. Phylogenomic analyses have consistently shown that stramenopiles and alveolates are closely related, but haptophytes and cryptophytes remain contentious; they have been proposed to branch together with several heterotrophic groups in the newly erected Hacrobia. Here, we tested this question by producing a large expressed sequence tag dataset for the katablepharid Roombia truncata, one of the last hacrobian lineages for which genome-level data are unavailable, and combined this dataset with the recently completed genome of the cryptophyte Guillardia theta to build an alignment composed of 258 genes. Our analyses strongly support haptophytes as sister to the SAR group, possibly together with telonemids and centrohelids. We also confirmed the common origin of katablepharids and cryptophytes, but these lineages were not related to other hacrobians; instead, they branch with plants. Our study resolves the evolutionary position of haptophytes, an ecologically critical component of the oceans, and proposes a new hypothesis for the origin of cryptophytes.

Evolutionary biologists have long sought to identify phenotypic traits whose evolution enhances an organism's performance in its environment. Diversification of traits related to resource acquisition can occur owing to spatial or temporal resource heterogeneity. We examined the ability to capture light in the Cryptophyta, a phylum of single-celled eukaryotic algae with diverse photosynthetic pigments, to better understand how acquisition of an abiotic resource may be associated with diversification. Cryptophytes originated through secondary endosymbiosis between an unknown eukaryotic host and a red algal symbiont. This merger resulted in distinctive pigment–protein complexes, the cryptophyte phycobiliproteins, which are the products of genes from both ancestors. These novel complexes may have facilitated diversification across environments where the spectrum of light available for photosynthesis varies widely. We measured light capture and pigments under controlled conditions in a phenotypically and phylogenetically diverse collection of cryptophytes. Using phylogenetic comparative methods, we found that phycobiliprotein characteristics were evolutionarily associated with diversification of light capture in cryptophytes, while non-phycobiliprotein pigments were not. Furthermore, phycobiliproteins were evolutionarily labile with repeated transitions and reversals. Thus, the endosymbiotic origin of cryptophyte phycobiliproteins provided an evolutionary spark that drove diversification of light capture, the resource that is the foundation of photosynthesis.

Photosynthetic organisms have developed diverse antennas composed of chromophorylated proteins to increase photon capture. Cryptophyte algae acquired their photosynthetic organelles (plastids) from a red alga by secondary endosymbiosis. Cryptophytes lost the primary red algal antenna, the red algal phycobilisome, replacing it with a unique antenna composed of αβ protomers, where the β subunit originates from the red algal phycobilisome. The origin of the cryptophyte antenna, particularly the unique α subunit, is unknown. Here we show that the cryptophyte antenna evolved from a complex between a red algal scaffolding protein and phycoerythrin β. Published cryo-EM maps for two red algal phycobilisomes contain clusters of unmodelled density homologous to the cryptophyte-αβ protomer. We modelled these densities, identifying a new family of scaffolding proteins related to red algal phycobilisome linker proteins that possess multiple copies of a cryptophyte-α-like domain. These domains bind to, and stabilise, a conserved hydrophobic surface on phycoerythrin β, which is the same binding site for its primary partner in the red algal phycobilisome, phycoerythrin α. We propose that after endosymbiosis these scaffolding proteins outcompeted the primary binding partner of phycoerythrin β, resulting in the demise of the red algal phycobilisome and emergence of the cryptophyte antenna. Cryptophytes acquired plastids from red algae but replaced the light-harvesting phycobilisome with a unique cryptophyte antenna. Here via analysis of phycobilisome cryo-EM structures, Rathbone et al. propose that the α subunit of the cryptophyte antenna originated from phycobilisome linker proteins

Anion channelrhodopsin from Guillardia theta ( Gt ACR1) has Asp234 (3.2 Å) and Glu68 (5.3 Å) near the protonated Schiff base. Here, we investigate mutant Gt ACR1s (e.g., E68Q/D234N) expressed in HEK293 cells. The influence of the acidic residues on the absorption wavelengths was also analyzed using a quantum mechanical/molecular mechanical approach. The calculated protonation pattern indicates that Asp234 is deprotonated and Glu68 is protonated in the original crystal structures. The D234E mutation and the E68Q/D234N mutation shorten and lengthen the measured and calculated absorption wavelengths, respectively, which suggests that Asp234 is deprotonated in the wild-type Gt ACR1. Molecular dynamics simulations show that upon mutation of deprotonated Asp234 to asparagine, deprotonated Glu68 reorients toward the Schiff base and the calculated absorption wavelength remains unchanged. The formation of the proton transfer pathway via Asp234 toward Glu68 and the disconnection of the anion conducting channel are likely a basis of the gating mechanism.

Cation channelrhodopsins, light-gated channels from flagellate green algae, are extensively used as optogenetic photoactivators of neurons in research and recently have progressed to clinical trials for vision restoration. However, the molecular mechanisms of their photoactivation remain poorly understood. We recently identified cryptophyte cation channelrhodopsins, structurally different from those of green algae, which have separately evolved to converge on light-gated cation conductance. This study reveals diversity within this new protein family and describes a subclade with unusually rapid desensitization that results in short transient photocurrents in continuous light. Such transient currents have not been observed in the green algae channelrhodopsins and are potentially useful in optogenetic protocols. Kinetic UV-visible (UV-vis) spectroscopy and photoelectrophysiology reveal that the desensitization is caused by rapid accumulation of a nonconductive photointermediate in the photochemical reaction cycle. The absorption maximum of the intermediate is 330 nm, the shortest wavelength reported in any rhodopsin, indicating a novel chromophore structure. Channelrhodopsins guide algal phototaxis and are widely used as optogenetic probes for control of membrane potential with light. “Bacteriorhodopsin-like” cation channelrhodopsins (BCCRs) from cryptophytes differ in primary structure from other CCRs, lacking usual residues important for their cation conductance. Instead, the sequences of BCCR match more closely those of rhodopsin proton pumps, containing residues responsible for critical proton transfer reactions. We report 19 new BCCRs which, together with the earlier 6 known members of this family, form three branches (subfamilies) of a phylogenetic tree. Here, we show that the conductance mechanisms in two subfamilies differ with respect to involvement of the homolog of the proton donor in rhodopsin pumps. Two BCCRs from the genus Rhodomonas generate photocurrents that rapidly desensitize under continuous illumination. Using a combination of patch clamp electrophysiology, absorption, Raman spectroscopy, and flash photolysis, we found that the desensitization is due to rapid accumulation of a long-lived nonconducting intermediate of the photocycle with unusually blue-shifted absorption with a maximum at 330 nm. These observations reveal diversity within the BCCR family and contribute to deeper understanding of their independently evolved cation channel function. IMPORTANCE Cation channelrhodopsins, light-gated channels from flagellate green algae, are extensively used as optogenetic photoactivators of neurons in research and recently have progressed to clinical trials for vision restoration. However, the molecular mechanisms of their photoactivation remain poorly understood. We recently identified cryptophyte cation channelrhodopsins, structurally different from those of green algae, which have separately evolved to converge on light-gated cation conductance. This study reveals diversity within this new protein family and describes a subclade with unusually rapid desensitization that results in short transient photocurrents in continuous light. Such transient currents have not been observed in the green algae channelrhodopsins and are potentially useful in optogenetic protocols. Kinetic UV-visible (UV-vis) spectroscopy and photoelectrophysiology reveal that the desensitization is caused by rapid accumulation of a nonconductive photointermediate in the photochemical reaction cycle. The absorption maximum of the intermediate is 330 nm, the shortest wavelength reported in any rhodopsin, indicating a novel chromophore structure.

Ecology and evolution unfold in spatially structured communities, where dispersal links dynamics across scales. Because dispersal is multicausal, identifying general drivers remains challenging. In a coordinated distributed experiment spanning organisms from protozoa to vertebrates, we tested whether two fundamental determinants of local dynamics, top-down and bottom-up control, generally explain active dispersal. We show that both factors consistently increased emigration rates and use metacommunity modelling to highlight consequences on local and regional dynamics. In a coordinated distributed dispersal experiment involving seven laboratories, the authors show that both top-down predation risk and bottom-up resource limitation increase emigration rates across 21 species ranging from protozoa to vertebrates.

Plants and algae have developed various regulatory mechanisms for optimal delivery of excitation energy to the photosystems even during fluctuating light conditions; these include state transitions as well as non-photochemical quenching. The former process maintains the balance by redistributing antennae excitation between the photosystems, meanwhile the latter by dissipating excessive excitation inside the antennae. In the present study, these mechanisms have been analysed in the cryptophyte alga Guillardia theta. Photoprotective non-photochemical quenching was observed in cultures only after they had entered the stationary growth phase. These cells displayed a diminished overall photosynthetic efficiency, measured as CO₂ assimilation rate and electron transport rate. However, in the logarithmic growth phase G. theta cells redistributed excitation energy via a mechanism similar to state transitions. These state transitions were triggered by blue light absorbed by the membrane integrated chlorophyll a/c antennae, and green light absorbed by the lumenal biliproteins was ineffective. It is proposed that state transitions in G. theta are induced by small re-arrangements of the intrinsic antennae proteins, resulting in their coupling/uncoupling to the photosystems in state 1 or state 2, respectively. G. theta therefore represents a chromalveolate algae able to perform state transitions.

Antarctic phototrophs are challenged by extreme temperatures, ice cover, nutrient limitation, and prolonged periods of darkness. Yet this environment may also provide niche opportunities for phytoplankton utilizing alternative nutritional modes. Mixotrophy, the combination of photosynthesis and particle ingestion, has been proposed as a mechanism for some phytoplankton to contend with the adverse conditions of the Antarctic. We conducted feeding experiments using fluorescent bacteria-sized tracers to compare the effects of light and nutrients on bacterivory rates in three Antarctic marine photosynthetic nanoflagellates representing two evolutionary lineages: Cryptophyceae (Geminigera cryophila) and Prasinophyceae (Pyramimonas tychotreta and Mantoniella antarctica). Only G. cryophila had previously been identified as mixotrophic. We also measured photoautotrophic abilities over a range of light intensities (P vs. I) and used dark survival experiments to assess cell population dynamics in the absence of light. Feeding behavior in these three nanoflagellates was affected by either light, nutrient levels, or a combination of both factors in a species-specific manner that was not conserved by evolutionary lineage. The different responses to environmental factors by these mixotrophs supported the idea of tradeoffs in the use of phagotrophy and phototrophy for growth.