Evolving paradigms in biological carbon cycling in the ocean

Zhang, Chuanlun; Dang, Hongyue; Azam, Farooq; Benner, Ronald; Legendre, Louis; Passow, Uta; Polimene, Luca; Robinson, Carol; Suttle, Curtis A.; Jiao, Nianzhi

doi:10.1093/nsr/nwy074

Cited by 123 publications

(86 citation statements)

References 145 publications

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“…It is challenging to define specific molecular properties that limit the microbial utilization of DOM (Zhang et al ), but advances in the chemical characterization of DOM are leading to new insights. Solid phase extraction methods used for the concentration and isolation of marine DOM, such as C‐18 used herein, commonly rely on a nonpolar stationary phase and hydrophobic interactions to preferentially adsorb mid‐ to nonpolar molecules from seawater (Benner ; Dittmar et al ).…”

Section: Discussionmentioning

confidence: 99%

Molecular properties are a primary control on the microbial utilization of dissolved organic matter in the ocean

Shen

Benner

2019

Limnology & Oceanography

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The global ocean sequesters a large amount of reduced carbon in dissolved organic molecules that can persist for centuries to millennia. The persistence of dissolved organic carbon (DOC) in the deep ocean has been attributed to inherently refractory molecules and to low concentrations of molecules, but the relative roles of molecular properties and molecular concentrations remain uncertain. We investigate both of these possibilities using bioassay experiments with unfiltered seawater collected from five depths (50-1500 m) at the Bermuda Atlantic Time-Series Study site. The microbial utilization of compositionally distinct forms of seawater DOC at in situ and elevated concentrations was determined. Microbial utilization of in situ organic carbon ranged from 6% to 7% in surface waters to 0% in deep water after 180 d. Additions of surface plankton-derived DOC (~18 μmol L −1 ), which was enriched in amino acids and carbohydrates, revealed substantial (50-75%) removal of the added DOC at all depths within 7 d. In sharp contrast, additions of C-18 isolated deep-sea DOC (~20 μmol L −1 ) showed insignificant or minimal utilization at all depths after 7 or 180 d, even when primed with labile substrates. These experiments demonstrate microbial communities from varying depths and environments in the ocean could rapidly utilize elevated concentrations of plankton-derived DOC, whereas these same microbes failed to utilize elevated concentrations of C-18 DOC. These results indicate molecular properties are the primary control on the microbial utilization of DOC in the ocean. Our findings imply a dynamic DOC reservoir with a flexible capacity for carbon sequestration in the global ocean.

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Section: Discussionmentioning

confidence: 99%

Molecular properties are a primary control on the microbial utilization of dissolved organic matter in the ocean

Shen

Benner

2019

Limnology & Oceanography

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“…Hence improved mechanistic understanding of the drivers influencing the variability of respiration, particularly those that are climate sensitive, or currently not represented in numerical models, is required. Examples would include the influence of changing inorganic nutrient concentrations and stoichiometry on plankton community structure including the proportion of respiration attributable to bacterioplankton or vertically migrating zooplankton and the size distribution and composition of exported particles, changes in the respiratory quotient, the interacting effects of increasing CO 2 and decreasing O 2 on bacterioplankton respiration, and the influence of warming and nutrient stoichiometry on the bacterial utilization of previously recalcitrant dissolved organic carbon (Jiao et al, 2010(Jiao et al, , 2014Zhang et al, 2018). On a broader scale, this complex wicked problem also requires an appreciation of the potential feedbacks between primary production, nitrogen cycling, organic matter flux and oxygen consumption (Canfield, 2006;Boyle et al, 2013;Bristow et al, 2016).…”

Section: Known Unknowns and Recommendations For Future Researchmentioning

confidence: 99%

Microbial Respiration, the Engine of Ocean Deoxygenation

Robinson

2019

Front. Mar. Sci.

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108

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Microbial plankton respiration is the key determinant in the balance between the storage of organic carbon in the oceans or its conversion to carbon dioxide with accompanying consumption of dissolved oxygen. Over the past 50 years, dissolved oxygen concentrations have decreased in many parts of the world's oceans, and this trend of ocean deoxygenation is predicted to continue. Yet despite its pivotal role in ocean deoxygenation, microbial respiration remains one of the least constrained microbial metabolic processes. Improved understanding of the magnitude and variability of respiration, including attribution to component plankton groups, and quantification of the respiratory quotient, would enable better predictions, and projections of the intensity and extent of ocean deoxygenation and of the integrative impact of ocean deoxygenation, ocean acidification, warming, and changes in nutrient concentration and stoichiometry on marine carbon storage. This study will synthesize current knowledge of respiration in relation to deoxygenation, including the drivers of its variability, identify key unknowns in our ability to project future scenarios and suggest an approach to move the field forward.

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“…The largest potential source of heterotrophic food in the oceans is dissolved organic matter (DOM) [12], but this food source is largely inaccessible to most marine animals. Instead, DOM is primarily utilized by heterotrophic microbes who recycle as much as 50% total marine productivity through the microbial loop [13].…”

Section: Introductionmentioning

confidence: 99%

Heterotrophy in the earliest gut: a single-cell view of heterotrophic carbon and nitrogen assimilation in sponge-microbe symbioses

et al. 2020

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Sponges are the oldest known extant animal-microbe symbiosis. These ubiquitous benthic animals play an important role in marine ecosystems in the cycling of dissolved organic matter (DOM), the largest source of organic matter on Earth. The conventional view on DOM cycling through microbial processing has been challenged by the interaction between this efficient filter-feeding host and its diverse and abundant microbiome. Here we quantify, for the first time, the role of host cells and microbial symbionts in sponge heterotrophy. We combined stable isotope probing and nanoscale secondary ion mass spectrometry to compare the processing of different sources of DOM (glucose, amino acids, algal-produced) and particulate organic matter (POM) by a high-microbial abundance (HMA) and low-microbial abundance (LMA) sponge with single-cell resolution. Contrary to common notion, we found that both microbial symbionts and host choanocyte (i.e. filter) cells and were active in DOM uptake. Although all DOM sources were assimilated by both sponges, higher microbial biomass in the HMA sponge corresponded to an increased capacity to process a greater variety of dissolved compounds. Nevertheless, in situ feeding data demonstrated that DOM was the primary carbon source for both the LMA and HMA sponge, accounting for ~90% of their heterotrophic diets. Microbes accounted for the majority (65–87%) of DOM assimilated by the HMA sponge (and ~60% of its total heterotrophic diet) but <5% in the LMA sponge. We propose that the evolutionary success of sponges is due to their different strategies to exploit the vast reservoir of DOM in the ocean.

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Evolving paradigms in biological carbon cycling in the ocean

Cited by 123 publications

References 145 publications

Molecular properties are a primary control on the microbial utilization of dissolved organic matter in the ocean

Molecular properties are a primary control on the microbial utilization of dissolved organic matter in the ocean

Microbial Respiration, the Engine of Ocean Deoxygenation

Heterotrophy in the earliest gut: a single-cell view of heterotrophic carbon and nitrogen assimilation in sponge-microbe symbioses

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