Physiology and Rates in Microbial Oceanography (PRIMO)
The need to understand how ocean global change affects marine life has exposed gaps in our knowledge of fundamental principles. Although molecular biological techniques, particularly ‘omics (genomics to proteomics), now dominate research in biological oceanography, physiological research has stagnated, leading to the assumption that physiology is outmoded. However, biological rates and biogeochemical fluxes remain the main currencies in biogeochemistry (BGC) models in which microbes play a central role. The question we aim to address – with a focus on marine microbes – is how to translate 'omics- based information on physiological potential into quantifiable physiological rates, and ultimately into BGC processes that can be represented in Earth system models.
While 'omics has revealed patterns in marine microbial diversity and metabolic pathways, it largely provides only static snapshots of physiological potential. Studies that weave ‘omics and physiological rates together provide greater insights and improved mechanistic understanding. But despite these advances, there is widespread frustration about the paucity of physiological metrics, as most of these metrics were devised before the molecular biology revolution. To improve our understanding of the roles of marine microbes in biogeochemical cycles, we need better tools to quantify physiological activity. Physiological rates quantify the integrated activity of proteins that drive marine BGC cycles and can bridge the gap between 'omics and biogeochemistry. We propose the development of a community and framework for co-designing physiological metrics as currency converters to link 'omics datasets and BGC models, a central aim of the international BioGeoSCAPES program.
The necessity to understand the influence of ocean global change on biota has exposed wide-ranging gaps in our knowledge of the fundamental principles that underpin marine life (Cooley et al., 2022). Concurrently, physiological research has stagnated, in part driven by the advent and subsequent rapid evolution of molecular biological techniques (i.e., ‘omics), such that they now influence all lines of enquiry in biological oceanography (Melzner et al., 2022). This dominance has led to an implicit assumption that physiology is outmoded, and that ecological and BGC models can be directly informed by ‘omics (Oremland et al., 2005). However, the main modeling currencies are biological rates and BGC fluxes. We propose, in this working group, to address the question: how do we translate the wealth of information on physiological potential and function from ‘omics-based studies to quantifiable physiological rates and, ultimately, to BGC processes and their representation in Earth system models?
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In marine science, over the last two decades, ‘omics has clearly demonstrated large-scale patterns in microbial diversity across oceanic provinces and provided insights into which metabolic pathways are active. The history of marine nitrogen fixation research reveals the benefits and limitations of physiological rate measurements, and also points to how these measurements can be complemented by more recent ‘omics approaches (Zehr and Capone, 2020). But, ‘omics-based approaches provide static ‘snap-shots' of physiological potential, and we need to improve our quantitative, process-level understanding of the roles of marine microbes in biogeochemical cycles. Indeed, it is physiological activity—as modified by biological species differences, environmental drivers, and the interactions between the two—that ultimately drives biogeochemical cycles (Falkowski et al., 2008).
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In contrast to the rapid evolution of ‘omics techniques, the physiological metrics used to quantify biological rates that are the cornerstones of BGC and Earth system models, such as primary productivity, have not fundamentally changed in decades (c.f. Boyd et al., 2022). ‘Omics provides a surfeit of data with immense potential to enhance our understanding, but at a level of detail that is often difficult to relate to the information provided by physiological rate measurements and the current need to better parameterize Earth system models (Meiler et al., 2022). This growing mismatch between the currencies of global-scale models (rates and fluxes) and the aspirations of omics (coupling cellular potential via ‘omics to Earth system model projections) must be addressed urgently if we are to understand the fundamental principles driving marine life and BGC cycles (Strzepek et al., 2022).
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Although our current choice of physiological metrics needs urgent scrutiny, there is compelling evidence of the utility of long-established (and overlooked) assays when interfaced with innovative phytoplankton cellular models (Inomura et al., 2020). But can we also be inventive and use ‘omics to interpret physiology in a more holistic way? Physiology can provide valuable insights into metabolism, even when considering only a few cellular processes. Imagine the progress in our fundamental understanding of the microbial ‘rules of life’ if we developed better metrics jointly with ‘omics.
Humanity needs us to be able to make accurate predictions about the current and future states of marine biogeochemical cycles now. Marine microbes drive most of the key marine biogeochemical cycles (Falkowski et al., 2008). Yet, our ability to predict the responses of marine microbes to complex climate change is currently limited, in part, by our inability to translate the ever-growing wealth of information we now have on physiological potential, gained from ‘omics, into an understanding of their activity. We need to capitalize on what we have already learned from the rare studies that have considered ‘omics and physiology jointly (e.g., Walworth et al., 2016).
We are now at cross-roads – if we don’t address the imbalance between the paucity of physiological metrics and their limited applicability to ‘omics urgently we may soon be at an impasse for the improved parameterization of ocean scale models needed to project the responses of microbes to complex climate change. The recent debate between the DARWIN modeling group from MiT (Meiler et al., 2022, 2023) and marine nitrogen fixation genomicists (Zehr and Riemann, 2023) reveals some of the emerging challenges in converting between ‘omics and modeling currencies that will become exacerbated if not addressed in a timely way. The need is clear, and the opportunity is now, but we have been hindered by disciplinary silos and language barriers between physiologists, molecular biologists, and modelers. This working group will serve the crucial role of getting these communities in the same room, organized around the common aim of connecting this great need to this great opportunity. The multi-disciplinary and international work we propose would be impossible to support from national or regional funding.