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1. Coral larvae increase nitrogen assimilation to stabilize algal symbiosis and combat bleaching under increased temperature

   https://doi.org/10.1371/journal.pbio.3002875  

   Huffmyer, Ariana S; Ashey, Jill; Strand, Emma; Chiles, Eric N; Su, Xiaoyang; Putnam, Hollie M (November 2024, PLOS Biology)

   Moran, Nancy A (Ed.)

   Rising sea surface temperatures are increasingly causing breakdown in the nutritional relationship between corals and algal endosymbionts (Symbiodiniaceae), threatening the basis of coral reef ecosystems and highlighting the critical role of coral reproduction in reef maintenance. The effects of thermal stress on metabolic exchange (i.e., transfer of fixed carbon photosynthates from symbiont to host) during sensitive early life stages, however, remains understudied. We exposed symbiotic Montipora capitata coral larvae in Hawaiʻi to high temperature (+2.5°C for 3 days), assessed rates of photosynthesis and respiration, and used stable isotope tracing (4 mM 13C sodium bicarbonate; 4.5 h) to quantify metabolite exchange. While larvae did not show any signs of bleaching and did not experience declines in survival and settlement, metabolic depression was significant under high temperature, indicated by a 19% reduction in respiration rates, but with no change in photosynthesis. Larvae exposed to high temperature showed evidence for maintained translocation of a major photosynthate, glucose, from the symbiont, but there was reduced metabolism of glucose through central carbon metabolism (i.e., glycolysis). The larval host invested in nitrogen cycling by increasing ammonium assimilation, urea metabolism, and sequestration of nitrogen into dipeptides, a mechanism that may support the maintenance of glucose translocation under thermal stress. Host nitrogen assimilation via dipeptide synthesis appears to be used for nitrogen limitation to the Symbiodiniaceae, and we hypothesize that nitrogen limitation contributes to retention of fixed carbon by favoring photosynthate translocation to the host. Collectively, our findings indicate that although these larvae are susceptible to metabolic stress under high temperature, diverting energy to nitrogen assimilation to maintain symbiont population density, photosynthesis, and carbon translocation may allow larvae to avoid bleaching and highlights potential life stage specific metabolic responses to stress. 

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2. Metabolic Remodeling during Biofilm Development of Bacillus subtilis

   https://doi.org/10.1128/mBio.00623-19  

   Pisithkul, Tippapha; Schroeder, Jeremy W.; Trujillo, Edna A.; Yeesin, Ponlkrit; Stevenson, David M.; Chaiamarit, Tai; Coon, Joshua J.; Wang, Jue D.; Amador-Noguez, Daniel; Ghigo, Jean-Marc; et al (June 2019, mBio)

   ABSTRACT Biofilms are structured communities of tightly associated cells that constitute the predominant state of bacterial growth in natural and human-made environments. Although the core genetic circuitry that controls biofilm formation in model bacteria such as Bacillus subtilis has been well characterized, little is known about the role that metabolism plays in this complex developmental process. Here, we performed a time-resolved analysis of the metabolic changes associated with pellicle biofilm formation and development in B. subtilis by combining metabolomic, transcriptomic, and proteomic analyses. We report surprisingly widespread and dynamic remodeling of metabolism affecting central carbon metabolism, primary biosynthetic pathways, fermentation pathways, and secondary metabolism. Most of these metabolic alterations were hitherto unrecognized as biofilm associated. For example, we observed increased activity of the tricarboxylic acid (TCA) cycle during early biofilm growth, a shift from fatty acid biosynthesis to fatty acid degradation, reorganization of iron metabolism and transport, and a switch from acetate to acetoin fermentation. Close agreement between metabolomic, transcriptomic, and proteomic measurements indicated that remodeling of metabolism during biofilm development was largely controlled at the transcriptional level. Our results also provide insights into the transcription factors and regulatory networks involved in this complex metabolic remodeling. Following upon these results, we demonstrated that acetoin production via acetolactate synthase is essential for robust biofilm growth and has the dual role of conserving redox balance and maintaining extracellular pH. This report represents a comprehensive systems-level investigation of the metabolic remodeling occurring during B. subtilis biofilm development that will serve as a useful road map for future studies on biofilm physiology. IMPORTANCE Bacterial biofilms are ubiquitous in natural environments and play an important role in many clinical, industrial, and ecological settings. Although much is known about the transcriptional regulatory networks that control biofilm formation in model bacteria such as Bacillus subtilis , very little is known about the role of metabolism in this complex developmental process. To address this important knowledge gap, we performed a time-resolved analysis of the metabolic changes associated with bacterial biofilm development in B. subtilis by combining metabolomic, transcriptomic, and proteomic analyses. Here, we report a widespread and dynamic remodeling of metabolism affecting central carbon metabolism, primary biosynthetic pathways, fermentation pathways, and secondary metabolism. This report serves as a unique hypothesis-generating resource for future studies on bacterial biofilm physiology. Outside the biofilm research area, this work should also prove relevant to any investigators interested in microbial physiology and metabolism. 

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3. Temporal evolution of single-cell transcriptomes of Drosophila olfactory projection neurons

   https://doi.org/10.7554/eLife.63450  

   Xie, Qijing; Brbic, Maria; Horns, Felix; Kolluru, Sai Saroja; Jones, Robert C; Li, Jiefu; Reddy, Anay R; Xie, Anthony; Kohani, Sayeh; Li, Zhuoran; et al (January 2021, eLife)

   null (Ed.)

   Neurons undergo substantial morphological and functional changes during development to form precise synaptic connections and acquire specific physiological properties. What are the underlying transcriptomic bases? Here, we obtained the single-cell transcriptomes of Drosophila olfactory projection neurons (PNs) at four developmental stages. We decoded the identity of 21 transcriptomic clusters corresponding to 20 PN types and developed methods to match transcriptomic clusters representing the same PN type across development. We discovered that PN transcriptomes reflect unique biological processes unfolding at each stage—neurite growth and pruning during metamorphosis at an early pupal stage; peaked transcriptomic diversity during olfactory circuit assembly at mid-pupal stages; and neuronal signaling in adults. At early developmental stages, PN types with adjacent birth order share similar transcriptomes. Together, our work reveals principles of cellular diversity during brain development and provides a resource for future studies of neural development in PNs and other neuronal types. 

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4. Parasitic ‘ Candidatus Aquarickettsia rohweri’ is a marker of disease susceptibility in Acropora cervicornis but is lost during thermal stress

   https://doi.org/10.1111/1462-2920.15245  

   Klinges, Grace; Maher, Rebecca_L; Vega_Thurber, Rebecca_L; Muller, Erinn_M (October 2020, Environmental Microbiology)

   Summary Holobiont phenotype results from a combination of host and symbiont genotypes as well as from prevailing environmental conditions that alter the relationships among symbiotic members. Corals exemplify this concept, where shifts in the algal symbiont community can lead to some corals becoming more or less thermally tolerant. Despite linkage between coral bleaching and disease, the roles of symbiotic bacteria in holobiont resistance and susceptibility to disease remains less well understood. This study thus characterizes the microbiome of disease‐resistant and ‐susceptibleAcropora cervicorniscoral genotypes (hereafter referred to simply as ‘genotypes’) before and after high temperature‐mediated bleaching. We found that the intracellular bacterial parasite ‘Ca.Aquarickettsia rohweri’ was strikingly abundant in disease‐susceptible genotypes. Disease‐resistant genotypes, however, had notably more diverse and even communities, with correspondingly low abundances of ‘Ca.Aquarickettsia’.Bleaching caused a dramatic reduction of ‘Ca.Aquarickettsia’ within disease‐susceptible corals and led to an increase in bacterial community dispersion, as well as the proliferation of opportunists. Our data support the hypothesis that ‘Ca.Aquarickettsia’ species increase coral disease risk through two mechanisms: (i) the creation of host nutritional deficiencies leading to a compromised host‐symbiont state and (ii) the opening of niche space for potential pathogens during thermal stress. 

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5. Nutrient dynamics in coral symbiosis depend on both the relative and absolute abundance of Symbiodiniaceae species

   https://doi.org/10.1186/s40168-022-01382-0  

   McIlroy, Shelby E.; terHorst, Casey P.; Teece, Mark; Coffroth, Mary Alice (December 2022, Microbiome)

   Abstract Background Symbionts provide a variety of reproductive, nutritional, and defensive resources to their hosts, but those resources can vary depending on symbiont community composition. As genetic techniques open our eyes to the breadth of symbiont diversity within myriad microbiomes, symbiosis research has begun to consider what ecological mechanisms affect the identity and relative abundance of symbiont species and how this community structure impacts resource exchange among partners. Here, we manipulated the in hospite density and relative ratio of two species of coral endosymbionts ( Symbiodinium microadriaticum and Breviolum minutum ) and used stable isotope enrichment to trace nutrient exchange with the host, Briareum asbestinum . Results The patterns of uptake and translocation of carbon and nitrogen varied with both density and ratio of symbionts. Once a density threshold was reached, carbon acquisition decreased with increasing proportions of S. microadriaticum . In hosts dominated by B. minutum , nitrogen uptake was density independent and intermediate. Conversely, for those corals dominated by S. microadriaticum , nitrogen uptake decreased as densities increased, and as a result, these hosts had the overall highest (at low density) and lowest (at high density) nitrogen enrichment. Conclusions Our findings show that the uptake and sharing of nutrients was strongly dependent on both the density of symbionts within the host, as well as which symbiont species was dominant. Together, these complex interactive effects suggest that host regulation and the repression of in hospite symbiont competition can ultimately lead to a more productive mutualism. 

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