Evidence for phosphonate usage in the coral holobiont

Phosphonates are characterized by a stable carbon-phosphorus bond and commonly occur as lipid conjugates in invertebrate cell membranes. Phosphonoacetate hydrolase encoded by the phnA gene, catalyses the cleavage of phosphonoacetate to acetate and phosphate. In this study, we demonstrate the unusually high phnA diversity in coral-associated bacteria. The holobiont of eight coral species tested positive when screened for phnA using degenerate primers. In two soft coral species, Sinularia and Discosoma, sequencing of the phnA gene showed 13 distinct groups on the basis of 90% sequence identity across 100% of the sequence. A total of 16 bacterial taxa capable of using phosphonoacetate as the sole carbon and phosphorus source were isolated; 8 of which had a phnA+ genotype. This study enhances our understanding of the wide taxonomic and environmental distribution of phnA, and highlights the importance of phosphonates in marine ecosystems. The ISME Journal (2010) 4, 45-461; doi:10.1038/ismej.2009.129; published online 3 December 2009

Fruit and Seed Volatiles: Multiple Stage Settings, Actors and Props in an Evolutionary Play

Plants emit volatile organic compounds (VOCs) from most parts of their anatomy. Conventionally, the volatiles of leaves, flowers, fruits and seeds have been investigated separately. This review presents an integrated perspective of volatiles produced by fruits and seeds in the context of selection on the whole plant. It suggests that fruit and seed volatiles may only be understood in the light of the chemistry of the whole plant. Fleshy fruit may be viewed as an ecological arena within which several evolutionary games are being played involving fruit VOCs. Fruit odour and colour may be correlated and interact via multimodal signalling in influencing visits by frugivores. The hypothesis of volatile crypsis in the evolution of hard seeds as protection against volatile diffusion and perception by seed predators is reviewed. Current views on the role of volatiles in ant dispersal of seeds or myrmecochory are summarised, especially the suggestion that ants are being manipulated by plants in the form of a sensory trap while providing this service. Plant VOC production is presented as an emergent phenotype that could result from multiple selection pressures acting on various plant parts; the ``plant'' phenotype and VOC profile may receive significant contributions from symbionts within the plant. Viewing the plant as a holobiont would benefit an understanding of the emergent plant phenotype.

Chlorophyll content and temperature-dependent net photosynthesis and respiration rate in the lichen Cetraria aculeata

We studied polar and temperate samples of the lichen Cetraria aculeata to investigate whether genetical differences between photobionts are correlated with physiological properties of the lichen holobiont. Net photosynthesis and dark respiration (DR) at different temperatures (from 0 to 30 °C) and photon flux densities (from 0 to 1,200 ?mol/m**2/s) were studied for four populations of Cetraria aculeata. Samples were collected from maritime Antarctica, Svalbard, Germany and Spain, representing different climatic situations. Sequencing of the photobiont showed that the investigated samples fall in the polar and temperate clade described in Fernández-Mendoza et al. (2011, doi:10.1111/j.1365-294X.2010.04993.x). Lichens with photobionts from these clades differ in their temperature optimum for photosynthesis, maximal net photosynthesis, maximal DR and chlorophyll content. Maximal net photosynthesis was much lower in Antarctica and Svalbard than in Germany and Spain. The difference was smaller when rates were expressed by chlorophyll content. The same is true for the temperature optima of polar (11 °C) and temperate (15 and 17 °C) lichens. Our results indicate that lichen mycobionts may adapt or acclimate to local environmental conditions either by selecting algae from regional pools or by regulating algal cell numbers (chlorophyll content) within the thallus.

Responses of the metabolism of the larvae of Pocillopora damicornis to ocean acidification and warming

Ocean acidification and warming are expected to threaten the persistence of tropical coral reef ecosystems. As coral reefs face multiple stressors, the distribution and abundance of corals will depend on the successful dispersal and settlement of coral larvae under changing environmental conditions. To explore this scenario, we used metabolic rate, at holobiont and molecular levels, as an index for assessing the physiological plasticity of Pocillopora damicornis larvae from this site to conditions of ocean acidity and warming. Larvae were incubated for 6 hours in seawater containing combinations of CO2 concentration (450 and 950 µatm) and temperature (28 and 30°C). Rates of larval oxygen consumption were higher at elevated temperatures. In contrast, high CO2 levels elicited depressed metabolic rates, especially for larvae released later in the spawning period. Rates of citrate synthase, a rate-limiting enzyme in aerobic metabolism, suggested a biochemical limit for increasing oxidative capacity in coral larvae in a warming, acidifying ocean. Biological responses were also compared between larvae released from adult colonies on the same day (cohorts). The metabolic physiology of Pocillopora damicornis larvae varied significantly by day of release. Additionally, we used environmental data collected on a reef in Moorea, French Polynesia to provide information about what adult corals and larvae may currently experience in the field. An autonomous pH sensor provided a continuous time series of pH on the natal fringing reef. In February/March, 2011, pH values averaged 8.075±0.023. Our results suggest that without adaptation or acclimatization, only a portion of naïve Pocillopora damicornis larvae may have suitable metabolic phenotypes for maintaining function and fitness in an end-of-the century ocean.

Ocean acidification rapidly reduces dinitrogen fixation associated with the hermatypic coral Seriatopora hystrix

Since productivity and growth of coral-associated dinoflagellate algae is nitrogen (N)-limited, dinitrogen (N2) fixation by coral-associated microbes is likely crucial for maintaining the coral-dinoflagellate symbiosis. It is thus essential to understand the effects future climate change will have on N2 fixation by the coral holobiont. This laboratory study is the first to investigate short-term effects of ocean acidification on N2 fixation activity associated with the tropical, hermatypic coral Seriatopora hystrix using the acetylene reduction assay in combination with calcification measurements. Findings reveal that simulated ocean acidification ( pCO2 1080 µatm) caused a rapid and significant decrease (53%) in N2 fixation rates associated with S. hystrix compared to the present day scenario ( pCO2 486 µatm). In addition, N2 fixation associated with the coral holobiont showed a positive exponential relationship with its calcification rates. This suggests that even small declines in calcification rates of hermatypic corals under high CO2 conditions may result in decreased N2 fixation activity, since these 2 processes may compete for energy in the coral holobiont. Ultimately, an intensified N limitation in combination with a decline in skeletal growth may trigger a negative feedback loop on coral productivity exacerbating the negative long-term effects of ocean acidification.

Intra-colonial response to Acroporid "White syndrome" lesions in tabular Acropora spp. (Scleractinia)

'White syndrome' is considered to be the most prevalent coral disease on the Great Barrier Reef, characterised by rapid rates of lesion progression and high levels of colony mortality. This study investigated the production and translocation of photoassimilates towards white syndrome lesions (WSLs) and artificially inflicted lesions in healthy and diseased colonies of tabular Acropora spp. to determine the intra-colonial response to white syndrome using C-14 labelling. Translocation of C-14 labelled photoassimilates was preferentially orientated away from active WSLs, with minimal C-14 activity observed in the lesion borders, whilst artificial lesions (ALs) created directly opposite WSL borders showed significantly higher C-14 activity, suggesting active translocation of photoassimilates for tissue regeneration. Transport of photoassimilates in healthy coral colonies was preferentially oriented towards ALs with a higher perimeter-area ratio, although translocation towards WSL boundaries was minimal even though the lesion perimeter was often the width of the colony (> 200 cm). We suggest that the preferential orientation of photoassimilates away from WSLs may represent a deliberate strategy by the colony to induce a 'shutdown reaction' in order to preserve intra-colonial resources within areas of the colony that are more likely to survive and recover.

Acclimatization of the tropical reef coral Acropora millepora to hyperthermal stress

The demise of reef-building corals potentially lies on the horizon, given ongoing climate change amid other anthropogenic environmental stressors. If corals cannot acclimatize or adapt to changing conditions, dramatic declines in the extent and health of the living reefs are expected within the next half century. The primary and proximal global threat to corals is climate change. Reef-building corals are dependent upon a nutritional symbiosis with photosynthetic dinoflagellates belonging to the group Symbiodinium. . The symbiosis between the cnidarian host and algal partner is a stress-sensitive relationship; temperatures just 1°C above normal thermal maxima can result in the breakdown of the symbiosis, resulting in coral bleaching (the loss of Symbiodinium and/or associated photopigments) and ultimately, colony death. As ocean temperatures continue to rise, corals will either acclimatize or adapt to changing conditions, or will perish. By experimentally preconditioning the coral Acropora millepora via sublethal heat treatment, the coral acquired thermal tolerance, resisting bleaching during subsequent hyperthermal stress. The complex nature of the coral holobiont translates to multiple possible explanations for acclimatization: acquired thermal tolerance could potentially originate from the host itself, the Symbiodinium, or from the bacterial community associated with the coral. By examining the type of in hospite Symbiodinium and the bacterial community prior acclimation and after thermal challenge, it is shown that short-term acclimatization is not due to a distinct change in the dinoflagellate or prokaryote community. Though the microbial partnerships remain without considerable flux in preconditioned corals, the host transcriptome is dynamic. One dominant pattern was the apparent tuning of gene expression observed between preconditioned and non-preconditioned treatments, showing a modulated transcriptomic response to stress. Additionally several genes were upregulated in association with thermal tolerance, including antiapoptotic genes, lectins, and oxidative stress response genes. Upstream of two of these thermal tolerance genes, inhibitor of NFκB and mannose-binding lectin, DNA polymorphisms were identified which vary significantly between the northern and southern Great Barrier Reef. The impact of these mutations in putative promoter regions remains to be seen, but variation across thermally-disparate geography serves to generate hypotheses regarding the role of regulatory element evolution in a coral adaptation context.