Stress-sensitive Species Research Articles

Seagrass meadows as ocean acidification refugia for sea urchin larvae

Foundation species have been widely documented to provide suitable habitats for other species by ameliorating stressful environmental conditions. Nonetheless, their role in rescuing stress-sensitive species from adverse conditions due to climate change remains often unexplored. Here, we performed a mesocosm experiment to assess whether the seagrass, Posidonia oceanica, through its photosynthetic activity, could mitigate the negative effects of ocean acidification on larval development and growth of the calcifying sea urchin, Paracentrotus lividus. Sea urchin larvae at early and late developmental stages that are generally associated to benthic habitats, were grown in aquaria with or without P. oceanica plants, under ambient or low pH conditions predicted by the end of the century under the worst climate scenario (RCP8.5). The percentage of abnormal larvae and their total body length under different experimental conditions were assessed on early- (i.e., pluteus; 72 h post-fertilization) and final-developmental stages (i.e., echinopluteus; 30 days post-fertilization), respectively. The presence of P. oceanica increased mean daily pH values of ∼0.1 and ∼0.15 units at ambient and low pH conditions, respectively, compared with tanks without plants. When grown at low pH in association with P. oceanica, plutei showed a ∼23 % reduction of malformations and echinoplutei a ∼34 % increase in total body length, respectively, compared with larvae developing in tanks without plants. Our results suggest that P. oceanica, by increasing pH and altering seawater carbonate chemistry through its metabolic activity, could buffer the negative effects of ocean acidification on calcifying organisms and could, thus, represent a tool against climate-driven loss of biodiversity.

Seven Years at High Salinity-Experimental Evolution of the Extremely Halotolerant Black Yeast Hortaea werneckii.

The experimental evolution of microorganisms exposed to extreme conditions can provide insight into cellular adaptation to stress. Typically, stress-sensitive species are exposed to stress over many generations and then examined for improvements in their stress tolerance. In contrast, when starting with an already stress-tolerant progenitor there may be less room for further improvement, it may still be able to tweak its cellular machinery to increase extremotolerance, perhaps at the cost of poorer performance under non-extreme conditions. To investigate these possibilities, a strain of extremely halotolerant black yeast Hortaea werneckii was grown for over seven years through at least 800 generations in a medium containing 4.3 M NaCl. Although this salinity is well above the optimum (0.8–1.7 M) for the species, the growth rate of the evolved H. werneckii did not change in the absence of salt or at high concentrations of NaCl, KCl, sorbitol, or glycerol. Other phenotypic traits did change during the course of the experimental evolution, including fewer multicellular chains in the evolved strains, significantly narrower cells, increased resistance to caspofungin, and altered melanisation. Whole-genome sequencing revealed the occurrence of multiple aneuploidies during the experimental evolution of the otherwise diploid H. werneckii. A significant overrepresentation of several gene groups was observed in aneuploid regions. Taken together, these changes suggest that long-term growth at extreme salinity led to alterations in cell wall and morphology, signalling pathways, and the pentose phosphate cycle. Although there is currently limited evidence for the adaptive value of these changes, they offer promising starting points for future studies of fungal halotolerance.

Positive cascading effects of epiphytes enhance the persistence of a habitat‐forming macroalga and the biodiversity of the associated invertebrate community under increasing stress

AbstractEnhanced persistence of stress sensitive species in harsh environments due to amelioration of physical stress by habitat‐forming species has been widely documented. By contrast, less attention has been given to positive species interactions that may enhance stress tolerance in habitat‐forming species, with positive cascading effects on biodiversity and ecosystem functioning.We used a combination of field surveys and experiments to assess the effects of the epiphyteJania rubens, on its subtidal macroalgal hostHalopithys incurva, and their cascading effects on the associated invertebrate community, along a depth gradient associated with increasing stress (i.e. light stress at shallower depths).Correlative studies showed that the biomass and photosynthetic efficiency ofH. incurvaincreased with depth, along with a decrease of epiphyte biomass. The experimental manipulation of epiphytes (removal in shallow water and addition in deep water) revealed that their effects onH. incurvaphysiology varied from positive in shallow habitats to negative in deep habitats. These results suggest that reduction of light/UV stress byJ. rubensallowsH. incurvato persist in shallow‐water habitats that would be otherwise unsuitable. In addition, colonization by large clumps ofJ. rubensincreased the abundance and diversity of associated invertebrates in shallow habitat, suggesting that positive feedbacks betweenH. incurva, acting as the primary habitat‐former, andJ. rubens, acting as a secondary habitat‐former, generate a facilitation cascade.Synthesis. Our study suggests that the persistence of some habitat‐forming species and their ability to support biodiversity may rely upon physical stress reduction by other species (e.g. epiphytes in our case) that are generally neglected when planning conservation strategies. A deeper understanding of context dependency in positive species interactions is essential for predicting patterns of species distribution under increasingly stressful climate scenarios.

English

Climate, fire and herbivory rank among the key factors and processes shaping savanna woodland community composition and diversity. We analyzed recruitment dynamics, community biomass, diversity, stability and composition and their relationships with rainfall fluctuations and herbivory in a savanna woodland community in the Masai Mara National Reserve of Kenya. Seedling and sapling recruitment varied differentially over time among the five commonest tree species. Rainfall exerted both positive and negative effects on recruitment dynamics, with saplings responding to longer rainfall lags than seedlings. The proportion of trees damaged by browsers peaked at intermediate rainfall levels and was higher for adults than seedlings or saplings. Community biomass, species richness and evenness increased with increasing rainfall. Biomass decreased, whereas richness and evenness hardly varied over time. Both rare and common species occurred in more diverse communities, prevalent at high rainfall locations, suggesting strong nestedness in community composition. Moreover, community stability and diversity appeared unrelated. Protection from browsers and lower per capita browsing pressure at high rainfall apparently enable rare species to successfully establish and elevate species diversity. If climate change makes droughts more frequent and intense and lowers soil moisture, browsing intensity could increase, reducing diversity and recruitment, especially of rare, stress-sensitive species. Key words: Masai Mara, species diversity, habitat filtering, rainfall, browsing, fire, competition, stochastic processes, tree biomass.

Harnessing positive species interactions as a tool against climate-driven loss of coastal biodiversity.

Habitat-forming species sustain biodiversity and ecosystem functioning in harsh environments through the amelioration of physical stress. Nonetheless, their role in shaping patterns of species distribution under future climate scenarios is generally overlooked. Focusing on coastal systems, we assess how habitat-forming species can influence the ability of stress-sensitive species to exhibit plastic responses, adapt to novel environmental conditions, or track suitable climates. Here, we argue that habitat-former populations could be managed as a nature-based solution against climate-driven loss of biodiversity. Drawing from different ecological and biological disciplines, we identify a series of actions to sustain the resilience of marine habitat-forming species to climate change, as well as their effectiveness and reliability in rescuing stress-sensitive species from increasingly adverse environmental conditions.

Plastid terminal oxidase requires translocation to the grana stacks to act as a sink for electron transport

The plastid terminal oxidase (PTOX) has been shown to be an important sink for photosynthetic electron transport in stress-tolerant plants. However, overexpression studies in stress-sensitive species have previously failed to induce significant activity of this protein. Here we show that overexpression of PTOX from the salt-tolerant brassica species Eutrema salsugineum does not, alone, result in activity, but that overexpressing plants show faster induction and a greater final level of PTOX activity once exposed to salt stress. This implies that an additional activation step is required before activity is induced. We show that that activation involves the translocation of the protein from the unstacked stromal lamellae to the thylakoid grana and a protection of the protein from trypsin digestion. This represents an important activation step and opens up possibilities in the search for stress-tolerant crops.

Directed diversity manipulations within natural phytoplankton communities

AbstractThere is general concern about the rapid decline in biodiversity. The consequences of biodiversity declines are expected to impact ecosystem functioning. Primary production is one of the ecosystem—functions where existing data already support such expectations. However, for a mechanistic understanding of these processes more experimental investigations are needed. In terrestrial primary producer communities a directed removal of species is one important tool in the experimental portfolio to study the consequences of a decline in biodiversity. However, this is notoriously difficult in suspended aquatic primary producer communities consisting of mostly unicellular phytoplankton. As phytoplankton are responsible for about 50% of global primary production, detailed knowledge of whether and how diversity declines will impact the functioning of natural phytoplankton communities is of crucial importance. Here, we tested two different methods, dilution and disturbance—to manipulate diversity of natural freshwater plankton communities along an experimental gradient in a directed way. Dilution will alter community composition by affecting mainly rare species whereas disturbance will affect mainly stress sensitive species. Both methods resulted in distinct and replicable species richness gradients. Such gradients enable the mechanistic study of general responses to biodiversity loss in natural phytoplankton communities with shared evolutionary history in an ecological meaningful way.

Environmental filtering and taxonomic relatedness underlie the species richness–evenness relationship

We examined the relationship between species richness (S) and evenness (J) within a novel, community assembly framework. We hypothesized that environmental stress leads to filtering (increasing the proportional abundance of tolerant species) and taxonomic dispersion (decreasing the number of species within genera and families). Environmental filtering would cause a decline in S by eliminating some stress-sensitive species and a reduction of J by allowing only tolerant species to maintain large populations. Taxonomic relatedness may influence both S and J by controlling the nature of interspecific interactions—positive under taxonomic dispersion versus negative under taxonomic clustering. Therefore, the S–J relationship may be a product of environmental filtering and taxonomic relatedness. We tested this framework with redundancy analyses and structural equation models using continental stream diatom and fish data. We confirmed that (i) environmental stress, defined by watershed forest cover, slope, and temperature, caused filtering (lower sensitive:tolerant species abundance ratios) and taxonomic dispersion (elevated genus:species richness and family:species richness ratios); (ii) S and J, which declined with filtering and taxonomic dispersion, exhibited a positive relationship; and (iii) the role of filtering on J was pronounced only under stressful conditions, while taxonomic dispersion remained an important predictor of J across stressful and favorable environments.

Extremophyte adaptations to salt and water deficit stress.

Plants that can survive and even thrive in extreme environments (extremophytes) are likely treasure boxes of plant adaptations to environmental stresses. These species represent excellent models for understanding mechanisms of stress tolerance that may not be present in stress-sensitive species, as well as for identifying genetic determinants to develop stress-tolerant crops. This special issue of Functional Plant Biology focuses on physiological and molecular processes that enable extremophytes to naturally survive high levels of salt or desiccation.

Community assembly in harsh environments: the prevalence of ecological drift in the heath vegetation of South America

Metacommunity dynamics is marked by a gradient ranging from pure ecological determinism to pure stochasticity. This gradient encompasses compositional turnover that is governed by ecological drift, selection and dispersal. Here we estimate the influences of selection, dispersal limitation acting in concert with drift, drift acting alone and homogenizing dispersal on the structure of tropical restinga heath vegetation growing under stressful conditions in north‐eastern South America. We hypothesize that if abiotic heterogeneity is strong enough, it could select distinct sets of colonizing species from neighbor ecosystems, with stress sensitive species occupying refuges created by abiotic heterogeneity and stress tolerators dominating the more exposed areas. In this case selection would occur at both biogeographical and local scales. Under its prevalence, we expect selection to have a major signature in the woody plant community structure in a phylogenetic null model. Alternatively, if abiotic heterogeneity is not strong enough to impose significant selection, the environment would be homogeneously stressful for the majority of species, and would be dominated species selected at biogeographical scale only. Under its prevalence, we expect drift to have a major signature in the phylogenetic null model. We used an analytical framework based on phylogenetic and community structure null models to assess the relative importance of ecological processes. We also aimed to characterize the ecosystem features that impose selection and dispersal limitation. We found that 95.1% of turnover in composition is attributable to drift, 2.4% to homogenizing dispersal, 2.1% to selection, and just 0.40% to dispersal limitation, thus confirming our Neutrality hypothesis. As expected, both soil and topographic variables influenced metacommunity structure. However, contrary to our prediction, light availability and vegetation structure were also important. The predominance of coarse spatial patterns correlated to topographic and soil properties suggests that coarse differences in wind exposure and associated vegetation and soil factors represent the main selective forces acting on the studied vegetation. The dominance of drift in the assembly of restinga heath vegetation is likely to result from homogeneously stressful environmental conditions and also from the ongoing colonization process that is taking place in the restinga by immigrants from species‐rich neighboring ecosystems.

Cultivation of shear stress sensitive and tolerant microalgal species in a tubular photobioreactor equipped with a centrifugal pump.

The tolerance to shear stress of Tetraselmis suecica, Isochrysis galbana, Skeletonema costatum, and Chaetoceros muelleri was determined in shear cylinders. The shear tolerance of the microalgae species strongly depends on the strain. I. galbana, S. costatum, and C. muelleri exposed to shear stress between 1.2 and 5.4 Pa resulted in severe cell damage. T. suecica is not sensitive to stresses up to 80 Pa. The possibility to grow these algae in a tubular photobioreactor (PBR) using a centrifugal pump for recirculation of the algae suspension was studied. The shear stresses imposed on the algae in the circulation tubes and at the pressure side of the pump were 0.57 and 1.82 Pa, respectively. The shear stress tolerant T. suecica was successfully cultivated in the PBR. Growth of I. galbana, S. costatum, and C. muelleri in the tubular PBR was not observed, not even at the lowest pumping speed. For the latter shear sensitive strains, the encountered shear stress levels were in the order of magnitude of the determined maximum shear tolerance of the algae. An equation was used to simulate the effect of possible damage of microalgae caused by passages through local high shear zones in centrifugal pumps on the total algae culture in the PBR. This simulation shows that a culture of shear stress sensitive species is bound to collapse after only limited number of passages, confirming the importance of considering shear stress as a process parameter in future design of closed PBRs for microalgal cultivation.

Genome Structures and Halophyte-Specific Gene Expression of the Extremophile Thellungiella parvula in Comparison with Thellungiella salsuginea (Thellungiella halophila) and Arabidopsis

The genome of Thellungiella parvula, a halophytic relative of Arabidopsis (Arabidopsis thaliana), is being assembled using Roche-454 sequencing. Analyses of a 10-Mb scaffold revealed synteny with Arabidopsis, with recombination and inversion and an uneven distribution of repeat sequences. T. parvula genome structure and DNA sequences were compared with orthologous regions from Arabidopsis and publicly available bacterial artificial chromosome sequences from Thellungiella salsuginea (previously Thellungiella halophila). The three-way comparison of sequences, from one abiotic stress-sensitive species and two tolerant species, revealed extensive sequence conservation and microcolinearity, but grouping Thellungiella species separately from Arabidopsis. However, the T. parvula segments are distinguished from their T. salsuginea counterparts by a pronounced paucity of repeat sequences, resulting in a 30% shorter DNA segment with essentially the same gene content in T. parvula. Among the genes is SALT OVERLY SENSITIVE1 (SOS1), a sodium/proton antiporter, which represents an essential component of plant salinity stress tolerance. Although the SOS1 coding region is highly conserved among all three species, the promoter regions show conservation only between the two Thellungiella species. Comparative transcript analyses revealed higher levels of basal as well as salt-induced SOS1 expression in both Thellungiella species as compared with Arabidopsis. The Thellungiella species and other halophytes share conserved pyrimidine-rich 5' untranslated region proximal regions of SOS1 that are missing in Arabidopsis. Completion of the genome structure of T. parvula is expected to highlight distinctive genetic elements underlying the extremophile lifestyle of this species.

Plants under Climatic Stress

An investigation has been made of the combined effects of low temperature and high light on the level of several photosynthetic products in the leaves of a group of plants differing widely in their tolerance to this stress. Starch levels in these plants after chilling are dependent on the time of day that temperatures are lowered and seem related to rates of CO(2) assimilation under this stress. Prolonged low-temperature, high-light treatment (10 C at 160 wm(-2)) of Sorghum bicolor induced a rapid starch hydrolysis after a lag of some 24 hours. Differing rates of starch loss at the cellular level and a rapid migration of chloroplasts toward the base of upper mesophyll cells were also seen in leaves of this stress-sensitive species.Chilling increased the level of almost all free amino acids in tolerant and in semi-tolerant species, while amino acids related to intermediates of the C(4)-pathway show a sharp or transitory decrease in Sorghum. These and other changes observed in Sorghum suggest that some time- and temperature-dependent blockages develop in the interconversion of C(4)-pathway intermediates and possibly in the flow of other intermediates to and from the sites of C(4)-photosynthesis.Levels of ATP in the leaves of Sorghum, Paspalum, and Amaranthus increased at night and following chilling and did not fall until pronounced necrosis of the leaves commenced.