Functional biogeography of marine microbial heterotrophs

Editor’s summary

In the ocean, the carbon cycle is driven mainly by microbial photosynthesis and respiration. Several processes sequester carbon at depth in labile and recalcitrant forms of dissolved organic carbon. Zakem et al. recognized that current biogeochemical models for the roles of microbial dynamics in ocean carbon storage are inadequate. To improve models, the authors harnessed available datasets from Pacific, Atlantic, and Indian Ocean transects to investigate the structure of oceanic microbial communities and then studied how this structure relates to function. At low latitudes, a vertical gradient can be discerned, with oligotrophs on the surface and increasingly copiotrophic populations at mesopelagic depths that avoid surface predation, grow slowly, and are key to regulating the amount of dissolved carbon stored in the ocean. 

Structured Abstract

INTRODUCTION

In the ocean, microorganisms dominate the processes of photosynthesis and respiration that cycle carbon between CO₂ and organic forms. However, the future trajectory of these processes and their impacts on ocean carbon sequestration in a changing ocean are uncertain. Heterotrophic prokaryotes (“heteroprokaryotes”) consume and respire organic carbon, but the complexity of their communities and organic substrates makes it difficult to mechanistically understand their structure and function. It remains unclear how to quantitatively represent heteroprokaryotic diversity at large scales and link this diversity with biogeochemical function and carbon storage processes. New genetic sequencing efforts in the ocean provide immense information about heteroprokaryotic communities, but new approaches are needed to connect this information with mechanistic marine ecosystem models.

RATIONALE

We synthesized sequencing data and mechanistic ecosystem modeling to study global-scale heteroprokaryotic functional diversity. We aggregated amplicon sequence variants (ASVs) from three ocean transects into 21 heteroprokaryotic guilds at the order level or higher, at which taxonomy broadly corresponds to function. We incorporated heteroprokaryotic diversity into a trait-based model with variable organic substrate lability and a metabolic trade-off between optimization for growth rate (copiotrophy) and substrate affinity (oligotrophy). We compared observed and modeled biogeographical patterns and used the model to diagnose the mechanisms producing them.

RESULTS

The biogeographical distributions of the heteroprokaryotic guilds revealed several reoccurring patterns. These patterns were highly consistent with those of the modeled communities. The model captured the poleward transition from oligotrophs (such as SAR11) to copiotrophs (such as Flavobacteriales) in surface waters. The modeled functional types consuming recalcitrant dissolved organic carbon (DOC) were excluded from the surface because of high grazing pressure. These types were predominantly copiotrophic, optimized for relatively fast growth, despite growing more slowly in absolute terms. The biogeographies of these “slow copiotrophs” matched those of many observed guilds (such as SAR324 and SAR202). We tested the model prediction that copiotrophy increases in the deep ocean by linking ASVs to genomes and developing a genome-based copiotrophy index. We found that many of the deep guilds did have higher degrees of copiotrophy despite lower maximum growth rates. Because these slow copiotrophs were excluded from surface waters, recalcitrant DOC accumulated, reproducing observed patterns and demonstrating that ecological interactions control surface DOC storage.

CONCLUSION

We generated a global-scale mechanistic understanding of marine heteroprokarytic functional diversity with observations and modeling. Our results indicated how shifts in microbial community composition drive respiration patterns, confirming that ecological dynamics matter for biological carbon storage. The resulting coarse-grained, mechanistic model of the marine microbiome will ultimately allow for more robust projections of carbon cycle feedbacks in a warming ocean.

Abstract

Heterotrophic bacteria and archaea (“heteroprokaryotes”) drive global carbon cycling, but how to quantitatively organize their functional complexity remains unclear. We generated a global-scale understanding of marine heteroprokaryotic functional biogeography by synthesizing genetic sequencing data with a mechanistic marine ecosystem model. We incorporated heteroprokaryotic diversity into the trait-based model along two axes: substrate lability and growth strategy. Using genetic sequences along three ocean transects, we compiled 21 heteroprokaryotic guilds and estimated their degree of optimization for rapid growth (copiotrophy). Data and model consistency indicated that gradients in grazing and substrate lability predominantly set biogeographical patterns, and we identified deep-ocean “slow copiotrophs” whose ecological interactions control the surface accumulation of dissolved organic carbon.