Camp, EF, Kahlke, T, Nitschke, MR, Varkey, D, Fisher, NL, Fujise, L, Goyen, S, Hughes, DJ, Lawson, CA, Ros, M, Woodcock, S, Xiao, K, Leggat, W & Suggett, DJ 2020, 'Revealing changes in the microbiome of Symbiodiniaceae under thermal stress.', Environmental microbiology.
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Symbiodiniaceae are a diverse family of marine dinoflagellates, well known as coral endosymbionts. Isolation and in vitro culture of Symbiodiniaceae strains for physiological studies is a widely adopted tool, especially in the context of understanding how environmental stress perturbs Symbiodiniaceae cell functioning. While the bacterial microbiomes of corals often correlate with coral health, the bacterial communities co-cultured with Symbiodiniaceae isolates have been largely overlooked, despite the potential of bacteria to significantly influence the emergent physiological properties of Symbiodiniaceae cultures. We examined the physiological response to heat stress by Symbiodiniaceae isolates (spanning three genera) with well-described thermal tolerances, and combined these observations with matched changes in bacterial composition and abundance through 16S rRNA metabarcoding. Under thermal stress, there were Symbiodiniaceae strain-specific changes in maximum quantum yield of photosystem II (proxy for health) and growth rates that were accompanied by changes in the relative abundance of multiple Symbiodiniaceae-specific bacteria. However, there were no Symbiodiniaceae-independent signatures of bacterial community reorganisation under heat stress. Notably, the thermally tolerant Durusdinium trenchii (ITS2 major profile D1a) had the most stable bacterial community under heat stress. Ultimately, this study highlights the complexity of Symbiodiniaceae-bacteria interactions and provides a first step towards uncoupling their relative contributions towards Symbiodiniaceae physiological functioning.
Camp, EF, Suggett, DJ, Pogoreutz, C, Nitschke, MR, Houlbreque, F, Hume, BCC, Gardner, SG, Zampighi, M, Rodolfo-Metalpa, R & Voolstra, CR 2020, 'Corals exhibit distinct patterns of microbial reorganisation to thrive in an extreme inshore environment', Coral Reefs.
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© 2020, Springer-Verlag GmbH Germany, part of Springer Nature. Climate change threatens the survival of scleractinian coral from exposure to concurrent ocean warming, acidification and deoxygenation; how corals can potentially adapt to this trio of stressors is currently unknown. This study investigates three coral species (Acropora muricata, Acropora pulchra and Porites lutea) dominant in an extreme mangrove lagoon (Bouraké, New Caledonia) where abiotic conditions exceed those predicted for many reef sites over the next 100 years under climate change and compared them to conspecifics from an environmentally more benign reef habitat. We studied holobiont physiology as well as plasticity in coral-associated microorganisms (Symbiodiniaceae and bacteria) through ITS2 and 16S rRNA sequencing, respectively. We hypothesised that differences in coral-associated microorganisms (Symbiodiniaceae and bacteria) between the lagoonal and adjacent reef habitats may support coral host productivity and ultimately the ability of corals to live in extreme environments. In the lagoon, all coral species exhibited a metabolic adjustment of reduced photosynthesis-to-respiration ratios (P/R), but this was accompanied by highly divergent coral host-specific microbial associations. This was substantiated by the absence of shared ITS2-type profiles (proxies for Symbiodiniaceae genotypes). We observed that ITS2 profiles originating from Durusdinium taxa made up < 3% and a novel Symbiodinium ITS2 profile A1-A1v associated with A. pulchra. Bacterial community profiles were also highly divergent in corals from the lagoonal environment, whereas corals from the reef site were consistently dominated by Hahellaceae, Endozoicomonas. As such, differences in host–microorganism associations aligned with different physiologies and habitats. Our results argue that a multitude of host–microorganism associations are required to fulfill the changing nutritional demands of corals persisting into environment...
Carney, RL, Brown, MV, Siboni, N, Raina, JB, Kahlke, T, Mitrovic, SM & Seymour, JR 2020, 'Highly heterogeneous temporal dynamics in the abundance and diversity of the emerging pathogens Arcobacter at an urban beach', Water Research, vol. 171.
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© 2019 While the significance of Arcobacter in clinical settings grows, the ecological dynamics of potentially pathogenic Arcobacter in coastal marine environments remains unclear. In this study, we monitored the temporal dynamics of Arcobacter at an urban beach subject to significant stormwater input and wet weather sewer overflows (WWSO). Weekly monitoring of bacterial communities over 24 months using 16S rRNA amplicon sequencing revealed large, intermittent peaks in the relative abundance of Arcobacter. Quantitative PCR was subsequently employed to track absolute abundance of Arcobacter 23S rRNA gene copies, revealing peaks in abundance reaching up to 108 gene copies L−1, with these increases statistically correlated with stormwater and WWSO intrusion. Notably, peaks in Arcobacter abundance were poorly correlated with enterococci plate counts, and remained elevated for one week following heavy rainfall. Using oligotyping we discriminated single nucleotide variants (SNVs) within the Arcobacter population, revealing 10 distinct clusters of SNVs that we defined as Arcobacter “ecotypes”, with each displaying distinct temporal dynamics. The most abundant ecotype during stormwater and modelled WWSO events displayed 16S rRNA sequence similarity to A. cryaerophilius, a species previously implicated in human illness. Our findings highlight the diverse environmental drivers of Arcobacter abundance within coastal settings and point to a potentially important, yet overlooked exposure risk of these potential pathogens to humans.
Collins, S, Boyd, PW & Doblin, MA 2020, 'Evolution, Microbes, and Changing Ocean Conditions', Annual review of marine science, vol. 12, pp. 181-208.
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Experimental evolution and the associated theory are underutilized in marine microbial studies; the two fields have developed largely in isolation. Here, we review evolutionary tools for addressing four key areas of ocean global change biology: linking plastic and evolutionary trait changes, the contribution of environmental variability to determining trait values, the role of multiple environmental drivers in trait change, and the fate of populations near their tolerance limits. Wherever possible, we highlight which data from marine studies could use evolutionary approaches and where marine model systems can advance our understanding of evolution. Finally, we discuss the emerging field of marine microbial experimental evolution. We propose a framework linking changes in environmental quality (defined as the cumulative effect on population growth rate) with population traits affecting evolutionary potential, in order to understand which evolutionary processes are likely to be most important across a range of locations for different types of marine microbes.
Fabris, M, George, J, Kuzhiumparambil, U, Lawson, CA, Jaramillo Madrid, AC, Abbriano, RM, Vickers, CE & Ralph, P 2020, 'Extrachromosomal genetic engineering of the marine diatom Phaeodactylum tricornutum enables the heterologous production of monoterpenoids.', ACS synthetic biology.
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Geraniol is a commercially-relevant plant-derived monoterpenoid that is a main component of rose essential oil and used as insect repellent. Geraniol is also a key intermediate compound in the biosynthesis of the monoterpenoid indole alkaloids (MIAs), a group of over 2,000 compounds that include high-value pharmaceuticals. As plants naturally produce extremely small amounts of these molecules and their chemical synthesis is complex, industrially sourcing these compounds is costly and inefficient. Hence, microbial hosts suitable to produce MIA precursors through synthetic biology and metabolic engineering are currently being sought. Here, we evaluated the suitability of an eukaryotic microalga, the marine diatom Phaeodactylum tricornutum, for the heterologous production of monoterpenoids. Profiling of endogenous metabolism revealed that P. tricornutum, unlike other microbes employed for industrial production of terpenoids, accumulates free pools of the precursor geranyl diphosphate. To evaluate the potential for larger synthetic biology applications, we engineered P. tricornutum through extrachromosomal, episome-based expression, for the heterologous biosynthesis of the MIA intermediate geraniol. By profiling the production of geraniol resulting from various genetic and cultivation arrangements, P. tricornutum reached the maximum geraniol titre of 0.309 mg/L in phototrophic conditions. This work provides i) a detailed analysis of P. tricornutum endogenous terpenoid metabolism, ii) a successful demonstration of extrachromosomal expression for metabolic pathway engineering with potential gene-stacking applications, and iii) a convincing proof-of-concept of the suitability of P. tricornutum as a novel production platform for heterologous monoterpenoids, with potential for complex pathway engineering aimed at the heterologous production of MIAs.
Hughes, DJ, Crosswell, JR, Doblin, MA, Oxborough, K, Ralph, PJ, Varkey, D & Suggett, DJ 2020, 'Dynamic variability of the phytoplankton electron requirement for carbon fixation in eastern Australian waters', JOURNAL OF MARINE SYSTEMS, vol. 202.
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Koren, K, Gravesen Salinas, NK, Santella, M, Moßhammer, M, Müller, MC, Dmitriev, RI, Borisov, SM, Kühl, M & Laursen, BW 2020, 'Evaluation of Ebselen-azadioxatriangulenium as redox-sensitive fluorescent intracellular probe and as indicator within a planar redox optode', Dyes and Pigments, vol. 173.
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© 2019 Redox homeostasis is essential for cellular survival and is therefore tightly regulated. Visualizing changes in the local redox state is essential for detecting oxidative stress, especially with the help of red, long emission lifetime probes. We synthesized a new reversible, redox-sensitive fluorescent probe, ebselen-azadioxatriangulenium (Ebselen-ADOTA), and characterized its potential use for intra- and extracellular redox sensing. The probe consists of a photostable triangulenium-based fluorophore (emission maximum at 564 nm) modulated by a redox-active ebselen motif. The reduced form only shows around 1/10 of the emission intensity of the oxidized form. The Ebselen-ADOTA probe exhibited reversible oxidation and reduction in solution under extracellular conditions. In addition, Ebselen-ADOTA can visualize an increase in oxidative stress within anaerobic bacteria when exposing them to air, the probe did not readily respond to changes in the redox environment inside mammalian cells, probably due to unfavorable localization, aggregation or binding to cysteine containing proteins. When incorporated inside a polymer matrix (hydrogel D4 mixed with poly(acrylic acid)), the probe showed a rapid and fully reversible response to redox changes, thus enabling the preparation of a redox-sensitive optode.
Kuhl, M, Trampe, E, Mosshammer, M, Johnson, M, Larkum, AWD, Frigaard, N-U & Koren, K 2020, 'Substantial near-infrared radiation-driven photosynthesis of chlorophyll f-containing cyanobacteria in a natural habitat', ELIFE, vol. 9.
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Liu, P-C, Peacock, WJ, Wang, L, Furbank, R, Larkum, A & Dennis, ES 2020, 'Leaf growth in early development is key to biomass heterosis in Arabidopsis.', Journal of experimental botany.
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Arabidopsis thaliana hybrids have similar properties to hybrid crops with greater biomass relative to the parents. We asked whether the greater biomass was due to increased photosynthetic efficiency per unit leaf area or to overall increased leaf area and increased total photosynthate per plant. We found that photosynthetic parameters (electron transport rate, CO2 assimilation rate, chlorophyll content, chloroplast number) were unchanged on a leaf unit area and unit fresh weight basis between parents and hybrids indicating that heterosis is not a result of increased photosynthetic efficiency. To investigate the possibility of increased leaf area producing more photosynthate per plant we studied C24/ Landsberg erecta (Ler) hybrids in detail. These hybrids have earlier germination and leaf growth than the parents leading to a larger leaf area at any point in development of the plant. The developing leaves of the hybrids are significantly larger than those of the parents with consequent greater production of photosynthate and an increased contribution to heterosis. The set of leaves contributing to heterosis changes as the plant develops; the four most recently emerged leaves make the greatest contribution. As a leaf matures, its contribution to heterosis attenuates. While photosynthesis per unit leaf area is unchanged at any stage of development in the hybrid, leaf area is greater and the amount of photosynthate per plant is increased.
Matthews, JL, Raina, J-B, Kahlke, T, Seymour, JR, van Oppen, MJH & Suggett, DJ 2020, 'Symbiodiniaceae-bacteria interactions: rethinking metabolite exchange in reef-building corals as multi-partner metabolic networks', ENVIRONMENTAL MICROBIOLOGY.
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Najafpour, MM, Zaharieva, I, Zand, Z, Maedeh Hosseini, S, Kouzmanova, M, Hołyńska, M, Tranca, I, Larkum, AW, Shen, J-R & Allakhverdiev, SI 2020, 'Water-oxidizing complex in Photosystem II: Its structure and relation to manganese-oxide based catalysts', Coordination Chemistry Reviews, vol. 409, pp. 213183-213183.
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Nguyen, LN, Commault, AS, Kahlke, T, Ralph, PJ, Semblante, GU, Johir, MAH & Nghiem, LD 2020, 'Genome sequencing as a new window into the microbial community of membrane bioreactors - A critical review', SCIENCE OF THE TOTAL ENVIRONMENT, vol. 704.
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Nguyen, LN, Truong, M, Nguyen, AQ, Johir, MAH, Commault, AS, Ralph, PJ, Semblante, GU & Nghiem, LD 2020, 'A sequential membrane bioreactor followed by a membrane microalgal reactor for nutrient removal and algal biomass production', ENVIRONMENTAL SCIENCE-WATER RESEARCH & TECHNOLOGY, vol. 6, no. 1, pp. 189-196.
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Osman, EO, Suggett, DJ, Voolstra, CR, Pettay, DT, Clark, DR, Pogoreutz, C, Sampayo, EM, Warner, ME & Smith, DJ 2020, 'Coral microbiome composition along the northern Red Sea suggests high plasticity of bacterial and specificity of endosymbiotic dinoflagellate communities', Microbiome, vol. 8, no. 1, p. 8.
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BACKGROUND: The capacity of reef-building corals to tolerate (or adapt to) heat stress is a key factor determining their resilience to future climate change. Changes in coral microbiome composition (particularly for microalgal endosymbionts and bacteria) is a potential mechanism that may assist corals to thrive in warm waters. The northern Red Sea experiences extreme temperatures anomalies, yet corals in this area rarely bleach suggesting possible refugia to climate change. However, the coral microbiome composition, and how it relates to the capacity to thrive in warm waters in this region, is entirely unknown. RESULTS: We investigated microbiomes for six coral species (Porites nodifera, Favia favus, Pocillopora damicornis, Seriatopora hystrix, Xenia umbellata, and Sarcophyton trocheliophorum) from five sites in the northern Red Sea spanning 4° of latitude and summer mean temperature ranges from 26.6 °C to 29.3 °C. A total of 19 distinct dinoflagellate endosymbionts were identified as belonging to three genera in the family Symbiodiniaceae (Symbiodinium, Cladocopium, and Durusdinium). Of these, 86% belonged to the genus Cladocopium, with notably five novel types (19%). The endosymbiont community showed a high degree of host-specificity despite the latitudinal gradient. In contrast, the diversity and composition of bacterial communities of the surface mucus layer (SML)-a compartment particularly sensitive to environmental change-varied significantly between sites, however for any given coral was species-specific. CONCLUSION: The conserved endosymbiotic community suggests high physiological plasticity to support holobiont productivity across the different latitudinal regimes. Further, the presence of five novel algal endosymbionts suggests selection of certain genotypes (or genetic adaptation) within the semi-isolated Red Sea. In contrast, the dynamic composition of bacteria associated with the SML across sites may contribute to holobiont function and broaden the e...
Pernice, M, Raina, JB, Rädecker, N, Cárdenas, A, Pogoreutz, C & Voolstra, CR 2020, 'Down to the bone: the role of overlooked endolithic microbiomes in reef coral health', ISME Journal, vol. 14, no. 2, pp. 325-334.
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© 2019, The Author(s). Reef-building corals harbour an astonishing diversity of microorganisms, including endosymbiotic microalgae, bacteria, archaea, and fungi. The metabolic interactions within this symbiotic consortium are fundamental to the ecological success of corals and the unique productivity of coral reef ecosystems. Over the last two decades, scientific efforts have been primarily channelled into dissecting the symbioses occurring in coral tissues. Although easily accessible, this compartment is only 2–3 mm thick, whereas the underlying calcium carbonate skeleton occupies the vast internal volume of corals. Far from being devoid of life, the skeleton harbours a wide array of algae, endolithic fungi, heterotrophic bacteria, and other boring eukaryotes, often forming distinct bands visible to the bare eye. Some of the critical functions of these endolithic microorganisms in coral health, such as nutrient cycling and metabolite transfer, which could enable the survival of corals during thermal stress, have long been demonstrated. In addition, some of these microorganisms can dissolve calcium carbonate, weakening the coral skeleton and therefore may play a major role in reef erosion. Yet, experimental data are wanting due to methodological limitations. Recent technological and conceptual advances now allow us to tease apart the complex physical, ecological, and chemical interactions at the heart of coral endolithic microbial communities. These new capabilities have resulted in an excellent body of research and provide an exciting outlook to further address the functional microbial ecology of the “overlooked” coral skeleton.
Rinke, C, Rubino, F, Messer, LF, Youssef, N, Parks, DH, Chuvochina, M, Brown, M, Jeffries, T, Tyson, GW, Seymour, JR & Hugenholtz, P 2020, 'Correction: A phylogenomic and ecological analysis of the globally abundant Marine Group II archaea (Ca. Poseidoniales ord. nov.).', The ISME journal.
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An amendment to this paper has been published and can be accessed via a link at the top of the paper.
Suggett, DJ, Edmondson, J, Howlett, L & Camp, EF 2020, 'Coralclip®: a low‐cost solution for rapid and targeted out‐planting of coral at scale', Restoration Ecology.
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Re‐attaching or out‐planting coral as fragments, colonies, and on larval settlement devices to substrates is a major bottleneck limiting scalabilty and viability of reef restoration practices. Many attachment approaches are in use, but none that are low‐cost, opportunistic, rapid but effective, for integration into existing tour operations on the Great Barrier Reef (GBR) where staff and boat time is a major cost and chemical fixatives cannot be easily used. We describe a novel attachment device—Coralclip®—developed to meet this need and so aid maintenance and restoration of GBR tourism sites. Coralclip® is a stainless steel springclip attached by a nail integrated through the spring coil, and can be deployed with a coral fragment in as fast as 15 seconds. Initial laboratory tests demonstrated that Coralclip® secured coral fragments or larval settlement tiles under dynamic flow regimes characteristic of exposed reefs. Coral out‐planting from fragments of opportunity and from nurseries (n = 4,580; 0.3–1.9 coral/minute; US$0.6–3.0/coral deployed) or larval settlement tiles (n = 400; 2.5 tiles/minute; US$0.5 tile deployed−1) when deployed by divers from routine boat operations at Opal Reef confirmed highly effective attachment, with ≤15% failure of clips found after 3–7 months. We discuss how Coralclip® is a cost‐effective means to support reef maintenance and restoration practices.
Sutherland, DL, Park, J, Heubeck, S, Ralph, PJ & Craggs, RJ 2020, 'Size matters – Microalgae production and nutrient removal in wastewater treatment high rate algal ponds of three different sizes', Algal Research, vol. 45.
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© 2019 Elsevier B.V. High rate algal ponds for coupled wastewater treatment and resource recovery have been the focus of much international research over the last 15 years. Microalgal biomass productivity reported in full-scale studies (1-ha or greater) have often been substantially lower than that reported from smaller scale ponds in similar climates, regardless of the season or the dominant microalgal species used. The disconnect between smaller-scale and full-scale productivity is unclear and uncertainty remains regarding the applicability of smaller scale studies to full-scale systems. In order to better understand the differences in reported productivity, the performance of three different size wastewater treatment high rate algal ponds (5 m2, 330 m2 and 1-ha) were assessed with respect to nutrient removal and microalgal productivity over three seasons. Both daily areal nutrient removal and biomass production were affected by the size of the pond. NH4-N removal via nitrification/denitrification decreased with increasing pond size, with the highest removal rate in the 5 m2 pond and the lowest in the 1-ha. Microalgal areal productivity was maximal in the 330 m2 pond, suggesting that a combination of mixing frequency and higher photosynthetic potential under low light conditions were the main drivers of enhanced productivity in this pond compared to the 5 m2 (mesocosm) and 1-ha (full-scale) ponds. The lowest daily nutrient removal and biomass production occurred in the 1-ha (full-scale) pond. Our results suggest that, based on the current design and operation of high rate algal ponds, the optimum size for maximum productivity is considerably smaller than the current full-scale systems. This has implications for commercial scale systems, with respect to capital and operational costs.
Teoh, F, Shah, B, Ostrowski, M & Paulsen, I 2020, 'Comparative membrane proteomics reveal contrasting adaptation strategies for coastal and oceanic marine Synechococcus cyanobacteria', ENVIRONMENTAL MICROBIOLOGY.
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Thackeray, SJ, Robinson, SA, Smith, P, Bruno, R, Kirschbaum, MUF, Bernacchi, C, Byrne, M, Cheung, W, Cotrufo, MF, Gienapp, P, Hartley, S, Janssens, I, Hefin Jones, T, Kobayashi, K, Luo, Y, Penuelas, J, Sage, R, Suggett, DJ, Way, D & Long, S 2020, 'Civil disobedience movements such as School Strike for the Climate are raising public awareness of the climate change emergency.', Global change biology.
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Trevathan-Tackett, SM, Jeffries, TC, Macreadie, PI, Manojlovic, B & Ralph, P 2020, 'Long-term decomposition captures key steps in microbial breakdown of seagrass litter.', The Science of the total environment, vol. 705, p. 135806.
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Seagrass biomass represents an important source of organic carbon that can contribute to long-term sediment carbon stocks in coastal ecosystems. There is little empirical data on the long-term microbial decomposition of seagrass detritus, despite this process being one of the key drivers of carbon-cycling in coastal ecosystems, that is, it influences the amount and quality of carbon available for sequestration. Here, our goal was to investigate how litter quality (leaf vs. rhizome/root) and the microbial communities involved in organic matter remineralisation shift over a 2-year field decomposition study north of Sydney, Australia using the temperate seagrass Zostera muelleri. The sites varied in bulk sediment characteristics and the sediment-associated microbial communities, but these variables overall had little influence on long-term seagrass decomposition rates or seagrass-associated microbiomes. The results showed a clear succession of bacterial and archaeal communities for both tissues types from r-strategists such as α- and γ-proteobacteria to K-strategies, including δ-proteobacteria, Bacteroidia and Spirochaetes. We used a new mathematical model to capture how decay rates varied over time and found that two decomposition events occurred for some seagrass leaf samples, possibly due to exudate input from living seagrass roots growing into the litter bag. The new model also indicated that conventional single exponential models overestimate long-term decay rates, and we detected for the first time the refractory, or stable, phase of decomposition for rhizome/root biomass. The stable phase began at approximately 20% mass remaining and after 600 days, and the persistence of rhizome/root biomass was attributed to the anoxic conditions and the preservation of refractory organic matter. While we predict that rhizome/root biomass will contribute more to the long-term sediment carbon stocks, the preservation of leaf carbon may be enhanced at locations were sedimenta...