Annual Review of Marine Science - Volume 14, 2022

The ability of marine organisms to thrive over wide ranges of environmental stressors that perturb structures of proteins, nucleic acids, and lipids illustrates the effectiveness of adaptation at the biochemical level. A critical role of these adaptations is to achieve a proper balance between structural rigidity, which is necessary for maintaining three-dimensional conformation, and flexibility, which is required to allow changes in conformation during function. The Goldilocks principle refers to this balancing act, wherein structural stability and functional properties are poised at values that are just right for the environment the organism faces. Achieving this balance involves changes in macromolecular sequence and adaptive change in the composition of the aqueous or lipid milieu in which macromolecules function. This article traces the development of the field of biochemical adaptation throughout my career and shows how comparative studies of marine animals from diverse habitats have shed light on fundamental properties of life common to all organisms.

To better understand life in the sea, marine scientists must first quantify how individual organisms experience their environment, and then describe how organismal performance depends on that experience. In this review, we first explore marine environmental variation from the perspective of pelagic organisms, the most abundant life forms in the ocean. Generation time, the ability to move relative to the surrounding water (even slowly), and the presence of environmental gradients at all spatial scales play dominant roles in determining the variation experienced by individuals, but this variation remains difficult to quantify. We then use this insight to critically examine current understanding of the environmental physiology of pelagic marine organisms. Physiologists have begun to grapple with the complexity presented by environmental variation, and promising frameworks exist for predicting and/or interpreting the consequences for physiological performance. However, new technology needs to be developed and much difficult empirical work remains, especially in quantifying response times to environmental variation and the interactions among multiple covarying factors. We call on the field of global-change biology to undertake these important challenges.

The ancient idea of the balance of nature continues to influence modern perspectives on global environmental change. Assumptions of stable biogeochemical steady states and linear responses to perturbation are widely employed in the interpretation of geochemical records. Here, we review the dynamics of the marine carbon cycle and its interactions with climate and life over geologic time, focusing on what the record of past changes can teach us about stability and instability in the Earth system. Emerging themes include the role of amplifying feedbacks in producing past carbon cycle disruptions, the importance of critical rates of change in the context of mass extinctions and potential Earth system tipping points, and the application of these ideas to the modern unbalanced carbon cycle. A comprehensive dynamical understanding of the marine record of global environmental disruption will be of great value in understanding the long-term consequences of anthropogenic change.

Marine ecosystems are increasingly impacted by global environmental changes, including warming temperatures, deoxygenation, and ocean acidification. Marine scientists recognize intuitively that these environmental changes are translated into community changes via organismal physiology. However, physiology remains a black box in many ecological studies, and coexisting species in a community are often assumed to respond similarly to environmental stressors. Here, we emphasize how greater attention to physiology can improve our ability to predict the emergent effects of ocean change. In particular, understanding shifts in the intensity and outcome of species interactions such as competition and predation requires a sharpened focus on physiological variation among community members and the energetic demands and trophic mismatches generated by environmental changes. Our review also highlights how key species interactions that are sensitive to environmental change can operate as ecological leverage points through which small changes in abiotic conditions are amplified into large changes in marine ecosystems.

Environmental pharmaceuticals represent a threat of emerging concern for marine ecosystems. Widely distributed and bioaccumulated, these contaminants could provoke adverse effects on aquatic organisms through modes of action like those reported for target species. In contrast to pharmacological uses, organisms in field conditions are exposed to complex mixtures of compounds with similar, different, or even opposing therapeutic effects. This review summarizes current knowledge of the main cellular pathways modulated by the most common classes of environmental pharmaceuticals occurring in marine ecosystems and accumulated by nontarget species—including nonsteroidal anti-inflammatory drugs, psychiatric drugs, cardiovascular and lipid regulator agents, steroidal hormones, and antibiotics—and describes an intricate network of possible interactions with both synergistic and antagonistic effects on the same cellular targets and metabolic pathways. This complexity reveals the intrinsic limits of the single-chemical approach to predict the long-term consequences and future impact of pharmaceuticals at organismal, population, and community levels.

Many large marine predators make excursions from surface waters to the deep ocean below 200 m. Moreover, the ability to access meso- and bathypelagic habitats has evolved independently across marine mammals, reptiles, birds, teleost fishes, and elasmobranchs. Theoretical and empirical evidence suggests a number of plausible functional hypotheses for deep-diving behavior. Developing ways to test among these hypotheses will, however, require new ways to quantify animal behavior and biophysical oceanographic processes at coherent spatiotemporal scales. Current knowledge gaps include quantifying ecological links between surface waters and mesopelagic habitats and the value of ecosystem services provided by biomass in the ocean twilight zone. Growing pressure for ocean twilight zone fisheries creates an urgent need to understand the importance of the deep pelagic ocean to large marine predators.

Environmental DNA (eDNA) is genetic material that has been shed from macroorganisms. It has received increased attention as an indirect marker for biodiversity monitoring. This article reviews the current status of eDNA metabarcoding (simultaneous detection of multiple species) as a noninvasive and cost-effective approach for monitoring marine fish communities and discusses the prospects for this growing field. eDNA metabarcoding coamplifies short fragments of fish eDNA across a wide variety of taxa and, coupled with high-throughput sequencing technologies, allows massively parallel sequencing to be performed simultaneously for dozens to hundreds of samples. It can predict species richness in a given area, detect habitat segregation and biogeographic patterns from small to large spatial scales, and monitor the spatiotemporal dynamics of fish communities. In addition, it can detect an anthropogenic impact on fish communities through evaluation of their functional diversity. Recognizing the strengths and limitations of eDNA metabarcoding will help ensure that continuous biodiversity monitoring at multiple sites will be useful for ecosystem conservation and sustainable use of fishery resources, possibly contributing to achieving the targets of the United Nations’ Sustainable Development Goal 14 for 2030.

A small subset of marine microbial enzymes and surface transporters have a disproportionately important influence on the cycling of carbon and nutrients in the global ocean. As a result, they largely determine marine biological productivity and have been the focus of considerable research attention from microbial oceanographers. Like all biological catalysts, the activity of these keystone biomolecules is subject to control by temperature and pH, leaving the crucial ecosystem functions they support potentially vulnerable to anthropogenic environmental change. We summarize and discuss both consensus and conflicting evidence on the effects of sea surface warming and ocean acidification for five of these critical enzymes [carbonic anhydrase, ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO), nitrogenase, nitrate reductase, and ammonia monooxygenase] and one important transporter (proteorhodopsin). Finally, we forecast how the responses of these few but essential biocatalysts to ongoing global change processes may ultimately help to shape the microbial communities and biogeochemical cycles of the future greenhouse ocean.

Approximately 45% of the photosynthetically fixed carbon on Earth occurs in the oceans in phytoplankton, which account for less than 1% of the world's photosynthetic biomass. This amazing empirical observation implies a very high photosynthetic energy conversion efficiency, but how efficiently is the solar energy actually used? The photon energy budget of photosynthesis can be divided into three terms: the quantum yields of photochemistry, fluorescence, and heat. Measuring two of these three processes closes the energy budget. The development of ultrasensitive, seagoing chlorophyll variable fluorescence and picosecond fluorescence lifetime instruments has allowed independent closure on the first two terms. With this closure, we can understand how phytoplankton respond to nutrient supplies on timescales of hours to months and, over longer timescales, to changes in climate.

The annual patterns of plankton succession in the ocean determine ecological and biogeochemical cycles. The temporally fluctuating interplay between photosynthetic eukaryotes and the associated microbiota balances the composition of aquatic planktonic ecosystems. In addition to nutrients and abiotic factors, chemical signaling determines the outcome of interactions between phytoplankton and their associated microbiomes. Chemical mediators control essential processes, such as the development of key morphological, physiological, behavioral, and life-history traits during algal growth. These molecules thus impact species succession and community composition across time and space in processes that are highlighted in this review. We focus on spatial, seasonal, and physiological dynamics that occur during the early association of algae with bacteria, the exponential growth of a bloom, and its decline and recycling. We also discuss how patterns from field data and global surveys might be linked to the actions of metabolic markers in natural phytoplankton assemblages.

The SUP05 clade of gammaproteobacteria (Thioglobaceae) comprises both primary producers and primary consumers of organic carbon in the oceans. Host-associated autotrophs are a principal source of carbon and other nutrients for deep-sea eukaryotes at hydrothermal vents, and their free-living relatives are a primary source of organic matter in seawater at vents and in marine oxygen minimum zones. Similar to other abundant marine heterotrophs, such as SAR11 and Roseobacter, heterotrophic Thioglobaceae use the dilute pool of osmolytes produced by phytoplankton for growth, including methylated amines and sulfonates. Heterotrophic members are common throughout the ocean, and autotrophic members are abundant at hydrothermal vents and in anoxic waters; combined, they can account for more than 50% of the total bacterial community. Studies of both cultured and uncultured representatives from this diverse family are providing novel insights into the shifting biogeochemical roles of autotrophic and heterotrophic bacteria that cross oxic–anoxic boundary layers in the ocean.

Quantitative imaging instruments produce a large number of images of plankton and marine snow, acquired in a controlled manner, from which the visual characteristics of individual objects and their in situ concentrations can be computed. To exploit this wealth of information, machine learning is necessary to automate tasks such as taxonomic classification. Through a review of the literature, we highlight the progress of those machine classifiers and what they can and still cannot be trusted for. Several examples showcase how the combination of quantitative imaging with machine learning has brought insights on pelagic ecology. They also highlight what is still missing and how images could be exploited further through trait-based approaches. In the future, we suggest deeper interactions with the computer sciences community, the adoption of data standards, and the more systematic sharing of databases to build a global community of pelagic image providers and users.

A key Earth system science question is the role of atmospheric deposition in supplying vital nutrients to the phytoplankton that form the base of marine food webs. Industrial and vehicular pollution, wildfires, volcanoes, biogenic debris, and desert dust all carry nutrients within their plumes throughout the globe. In remote ocean ecosystems, aerosol deposition represents an essential new source of nutrients for primary production. The large spatiotemporal variability in aerosols from myriad sources combined with the differential responses of marine biota to changing fluxes makes it crucially important to understand where, when, and how much nutrients from the atmosphere enter marine ecosystems. This review brings together existing literature, experimental evidence of impacts, and new atmospheric nutrient observations that can be compared with atmospheric and ocean biogeochemistry modeling. We evaluate the contribution and spatiotemporal variability of nutrient-bearing aerosols from desert dust, wildfire, volcanic, and anthropogenic sources, including the organic component, deposition fluxes, and oceanic impacts.

The large-scale dynamics of ocean oxygenation have changed dramatically throughout Earth's history, in step with major changes in the abundance of O2 in the atmosphere and changes to marine nutrient availability. A comprehensive mechanistic understanding of this history requires insights from oceanography, marine geology, geochemistry, geomicrobiology, evolutionary ecology, and Earth system modeling. Here, we attempt to synthesize the major features of evolving ocean oxygenation on Earth through more than 3 billion years of planetary history. We review the fundamental first-order controls on ocean oxygen distribution and summarize the current understanding of the history of ocean oxygenation on Earth from empirical and theoretical perspectives—integrating geochemical reconstructions of oceanic and atmospheric chemistry, genomic constraints on evolving microbial metabolism, and mechanistic biogeochemical models. These changes are used to illustrate primary regimes of large-scale ocean oxygenation and to highlight feedbacks that can act to stabilize and destabilize the ocean–atmosphere system in anoxic, low-oxygen, and high-oxygen states.

Organic matter (OM) plays a significant role in the formation of oxygen minimum zones (OMZs) and associated biogeochemical cycling. OM supply processes to the OMZ include physical transport, particle formation, and sinking as well as active transport by migrating zooplankton and nekton. In addition to the availability of oxygen and other electron acceptors, the remineralization rate of OM is controlled by its biochemical quality. Enhanced microbial respiration of OM can induce anoxic microzones in an otherwise oxygenated water column. Reduced OM degradation under low-oxygen conditions, on the other hand, may increase the CO2 storage time in the ocean. Understanding the interdependencies between OM and oxygen cycling is of high relevance for an ocean facing deoxygenation as a consequence of global warming. In this review, we describe OM fluxes into and cycling within two large OMZs associated with eastern boundary upwelling systems that differ greatly in the extent of oxygen loss: the highly oxygen-depleted OMZ in the tropical South Pacific and the moderately hypoxic OMZ in the tropical North Atlantic. We summarize new findings from a large German collaborative research project, Collaborative Research Center 754 (SFB 754), and identify knowledge gaps and future research priorities.

Argo, an international, global observational array of nearly 4,000 autonomous robotic profiling floats, each measuring ocean temperature and salinity from 0 to 2,000 m on nominal 10-day cycles, has revolutionized physical oceanography. Argo started at the turn of the millennium,growing out of advances in float technology over the previous several decades. After two decades, with well over 2 million profiles made publicly available in real time, Argo data have underpinned more than 4,000 scientific publications and improved countless nowcasts, forecasts, and projections. We review a small subset of those accomplishments, such as elucidating remarkable zonal jets spanning the deep tropical Pacific; increasing understanding of ocean eddies and the roles of mixing in shaping water masses and circulation; illuminating interannual to decadal ocean variability; quantifying, in concert with satellite data, contributions of ocean warming and ice melting to sea level rise; improving coupled numerical weather predictions; and underpinning decadal climate forecasts.

Ocean ventilation is the transfer of tracers and young water from the surface down into the ocean interior. The tracers that can be transported to depth include anthropogenic heat and carbon, both of which are critical to understanding future climate trajectories. Ventilation occurs in both high- and midlatitude regions, but it is the southern midlatitudes that are responsible for the largest fraction of anthropogenic heat and carbon uptake; such Southern Ocean ventilation is the focus of this review. Southern Ocean ventilation occurs through a chain of interconnected mechanisms, including the zonally averaged meridional overturning circulation, localized subduction, eddy-driven mixing along isopycnals, and lateral transport by subtropical gyres. To unravel the complex pathways of ventilation and reconcile conflicting results, here we assess the relative contribution of each of thesemechanisms, emphasizing the three-dimensional and temporally varying nature of the ventilation of the Southern Ocean pycnocline. We conclude that Southern Ocean ventilation depends on multiple processes and that simplified frameworks that explain ventilation changes through a single process are insufficient.

Aquatic eddy covariance (AEC) is increasingly being used to study benthic oxygen (O2) flux dynamics, organic carbon cycling, and ecosystem health in marine and freshwater environments. Because it is a noninvasive technique, has a high temporal resolution (∼15 min), and integrates over a large area of the seafloor (typically 10–100 m²), it has provided new insights on the functioning of aquatic ecosystems under naturally varying in situ conditions and has given us more accurate assessments of their metabolism. In this review, we summarize biogeochemical, ecological, and biological insightsgained from AEC studies of marine ecosystems. A general finding for all substrates is that benthic O2 exchange is far more dynamic than earlier recognized, and thus accurate mean values can only be obtained from measurements that integrate over all timescales that affect the local O2 exchange. Finally, we highlight new developments of the technique, including measurements of air–water gas exchange and long-term deployments.

This review focuses on recent advances in process-based numerical models of the impact of extreme storms on sandy coasts. Driven by larger-scale models of meteorology and hydrodynamics, these models simulate morphodynamics across the Sallenger storm-impact scale, including swash,collision, overwash, and inundation. Models are becoming both wider (as more processes are added) and deeper (as detailed physics replaces earlier parameterizations). Algorithms for wave-induced flows and sediment transport under shoaling waves are among the recent developments. Community and open-source models have become the norm. Observations of initial conditions (topography, land cover, and sediment characteristics) have become more detailed, and improvements in tropical cyclone and wave models provide forcing (winds, waves, surge, and upland flow) that is better resolved and more accurate, yielding commensurate improvements in model skill. We foresee that future storm-impact models will increasingly resolve individual waves, apply data assimilation, and be used in ensemble modeling modes to predict uncertainties.