Marine microbes in a changing climate

Events of the last few years have made Professor Dyhrman think about community resilience in new ways, both for human societies and for phytoplankton communities and the ecosystems they support. Roughly 50 Pg of carbon per year is fixed into organic forms by phytoplankton in the surface ocean and this resulting chemical-microbe network underpins ocean ecosystem structure and function. So-called ‘omic approaches are providing critical insight into how culture isolates, simple-communities, and even the complex field systems that represent this network can be driven by biotic factors like microbial interactions and abiotic factors such as temperature, resource availability, and CO₂ concentration among other factors. Yet, the over-arching rules that govern these processes are poorly constrained and this adds to the myriad challenges in predicting future ocean patterns in microbial diversity and biogeochemistry. What are the key drivers that shape the chemical – microbe network? How sensitive is this network to a changing ocean?  Here Professor Dyhrman will discuss field observations of microbial physiological ecology and the drivers of these patterns in the surface ocean. Leveraging multi-‘omic approaches the group is working to understand the drivers of phytoplankton diversity and activities in the chemical-microbe network. Moving beyond previous methodological constraints, and single domain perspectives, there is a confluence of need and opportunity to more fully resolve the rules which govern the chemical – microbe network in  the ocean. She will highlight the perspectives that come from our community discussion in this area. Collectively, this knowledge will help better predict marine ecosystem resiliency on a changing planet.

Earth System Models (ESMs) play a crucial role in assessing impacts on ocean biogeochemistry and biology in the global ocean. However, ESM projections of biological change neglect the growing insight from genomic datasets. Instead, metabolic models arise from advances in Systems Biology. They focus on the molecular functioning of organisms under different environmental conditions, suggesting that integrating ESMs with metabolic models would improve our ability to deliver a molecular, ecological, and evolutionary understanding of the links between environmental change and the phenology of organisms. This talk presents recent computational modelling that abstract the metabolic network capacity called the metabolic niche. This new formal definition of the fundamental niche is based on the genome-scale description of a given organism. It approximates the capacity of an organism to survive based on nutrient availability. It shows that the presence-absence of genes is insufficient to describe the niche and metabolic niche modelling allows for the investigation of the most important reactions for organisms survival of emblematic organisms such as diatoms or cyanobacteria. When intertwined with ESMs, the same concept predicts plankton's global scale metabolite production and the molecular response of organisms to environmental changes. In particular, these results highlight several acclimation strategies occurring globally that are characterized by nutritional stresses and their physiological consequences for maintaining growth rates. These include critical phenotypic traits such as energy storage via glycogen or lipids or mixotrophy, neglected so far by ESMs. This talk will demonstrate the potential of integrating genomic knowledge into biogeochemical modelling for including adaptation and evolutionary mechanisms in climate studies.

This talk presents the results of a project that aimed to understand the hidden molecular mechanisms underlying intraspecific thermal micro-diversity within a single coastal Synechococcus population. An estuarine microbial assemblage was collected, and incubated at 18^oC and 30^oC for two weeks to allow thermal selection and strain sorting to occur. Clonal Synechococcus isolates were then obtained from both temperature treatments using flow cytometry, and their thermal response curves were characterized in the laboratory. Isolates from the low and high temperature incubations were morphologically identical but thermally distinct, consisting of 'cool' or 'warm' thermotypes, respectively, based on their significantly different thermal optimum and upper thermal limit traits. These two contrasting Synechococcus thermotypes also exhibited consistent temperature-dependent differences in photobiology. Illumina sequencing was however completely unable to distinguish between these two thermally-divergent strains, with >99.9% average nucleotide identity across all the isolates. Application of long read sequencing technology ultimately showed that the relevant thermal adaptation mechanisms were not genomic at all, but differences in the two thermotypes instead correlated with m-5 cytosine methylation of the genes coding for C-phycocyanin. This thermally-significant epigenomic difference would be invisible to studies based on amplicon sequencing or metagenomics, and yet such cryptic, non-genomic, intra-specific micro-diversity could play a key role in providing thermal resiliency to cyanobacteria populations growing in a warming ocean. 

Understanding the response of microbes to ocean global change requires an improved grasp of their underlying metabolic mechanisms, along with enhanced awareness of how altered microbial performance influences ocean biogeochemistry and ecology. Molecular biology offers a step change in the flow of information on the physiological potential of microbes. However, this unprecedented detail has been very difficult to translate into wider biogeochemical or ecological ramifications. To commence, Professor Boyd will make the case for a renewed focus on physiological rate measurements that is driven by the co-design of new ‘fit-for-purpose’ metrics by the omics and physiology research communities. Such metrics can help bridge the gap between omics and biogeochemistry.  Later, he will illustrate the need for a physiological ‘currency converter’ – by examining the wide-ranging strategies microbes employ to obtain fluctuating resources over the diurnal cycle. The superimposition of biological rhythms upon environmental heterogeneity poses major challenges for ocean sampling. There is emerging evidence of diel cycles across transcriptomics to lipidomics that brings important insights to the prior physiologically-based literature on the influence of diurnal cycles on ocean biogeochemistry. How can we best sample the ocean in a way that enables microbial metabolic responses to be understood mechanistically, then linked to the wider microbial community dynamics and their biogeochemical roles? New high-resolution datasets from robotic profiling floats, with both environmental and bio-optical sensors, may offer a framework to devise optimal sampling strategies for omics, rates, and biogeochemical fluxes.

Numerically abundant marine microbes hold great promise as model organisms for studying the ocean's response to a changing climate. Laboratory isolates representing genetically distinct lineages within the Prochlorococcus and SAR11 collectives have been essential in providing genetic reference information, linking genomic potential to physiological processes, and testing theories that arise from environmental sequences. The recent isolation of novel lineages from these collectives and the creation of stable semi-continuous co-cultures are expanding the utility of these organisms to inform our understanding of energy flow in the marine environment.

With substantial proportions of environmental sequence data still exhibiting poor recruitment to reference databases, Assistant Professor Becker will highlight what they believe to be the continued importance of domesticating wild marine microbes. They will define an appropriate level of taxonomic specificity for predicting microbial responses to global change (or not) and explore the potential of democratized sequencing for making informed sampling decisions at sea. They will look at several instances where laboratory isolates transformed our understanding of marine biogeochemical cycling before considering what knowledge gaps still exist as we navigate the bumpy journey from genome to biome. 

Finally, Assistant Professor Becker will share some nascent thoughts on pedagogical approaches to equip the next generation of oceanographers, modellers, and computational biologists with the necessary tools to collaborate with Earth's microbes and maintain a habitable Earth.

Microorganisms are primary drivers of biogeochemical cycles and thus centrally important for maintaining Earth as a habitable environment, but much remains unknown about their biogeography, controls on distribution, and metabolic potential and exchanges. Given multiple concurrent human- and climate-driven perturbations to the ocean environment, the habitats that exist now may be considerably different in only 10–15 years – predicting these shifts is essential to inform management and decision-making. As a result, there is an urgent need to elucidate interactions between microbes and their biogeochemical environments. In recent years, an international community effort has been underway to design a global-scale marine microbial biogeochemistry program 'BioGeoSCAPES: Ocean Metabolism and Nutrient Cycles on a Changing Planet' that combines rich biological (nucleic acid- and chemical omics) and chemical (nutrients, micronutrients, metabolites) sampling to map microbial communities and study ocean metabolism and its influence on ecosystem health and biogeochemical cycles. Recent advances in analytical and bioinformatics capabilities, combined with community-based momentum to organise ‘omics intercalibration and standardisation activities make this the ideal time to act. Dr Twining will describe a recently funded US NSF project to support planning and development of BioGeoSCAPES through a combination of meetings, workshops, working groups, student and postdoc exchanges, and summer school events. Planned community activities are envisioned to result in an international science plan, as well as plans for intercalibration assessment, methodological and sampling best practices, data management and informatics, and data-model integration strategies.