Abstract

Microorganisms in marine sediments play major roles in marine biogeochemical cycles by mineralizing substantial quantities of organic matter from decaying cells. Proteins and lipids are abundant components of necromass, yet the taxonomic identities of microorganisms that actively degrade them remain poorly resolved. Here, we revealed identities, trophic interactions, and genomic features of bacteria that degraded 13C-labeled proteins and lipids in cold anoxic microcosms containing sulfidic subarctic marine sediment. Supplemented proteins and lipids were rapidly fermented to various volatile fatty acids within 5 days. DNA-stable isotope probing (SIP) suggested Psychrilyobacter atlanticus was an important primary degrader of proteins, and Psychromonas members were important primary degraders of both proteins and lipids. Closely related Psychromonas populations, as represented by distinct 16S rRNA gene variants, differentially utilized either proteins or lipids. DNA-SIP also showed 13C-labeling of various Deltaproteobacteria within 10 days, indicating trophic transfer of carbon to putative sulfate-reducers. Metagenome-assembled genomes revealed the primary hydrolyzers encoded secreted peptidases or lipases, and enzymes for catabolism of protein or lipid degradation products. Psychromonas species are prevalent in diverse marine sediments, suggesting they are important players in organic carbon processing in situ. Together, this study provides new insights into the identities, functions, and genomes of bacteria that actively degrade abundant necromass macromolecules in the seafloor.

Highlights

  • IntroductionThe majority of marine sediments that underlie the Earth’s oceans are dominated by heterotrophic microorganisms, which are primarily sustained by “pelagic-benthic” coupling [1]

  • The majority of marine sediments that underlie the Earth’s oceans are dominated by heterotrophic microorganisms, which are primarily sustained by “pelagic-benthic” coupling [1]. This is driven by a constant supply of organic matter from planktonic organisms that thrive in the overlying water column and settle with particulate aggregates to the seafloor after their death [2]

  • Sulfate removal and volatile fatty acid turnover during protein and lipid degradation Sulfate was largely turned over after 48 days in all incubation treatments, except in incubations where sulfate reduction was inhibited by molybdate, where it remained between 18.1 and 24.2 mM (Fig. 1A)

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Summary

Introduction

The majority of marine sediments that underlie the Earth’s oceans are dominated by heterotrophic microorganisms, which are primarily sustained by “pelagic-benthic” coupling [1] This is driven by a constant supply of organic matter from planktonic organisms that thrive in the overlying water column and settle with particulate aggregates to the seafloor after their death [2]. Lipids generally consist of an alkyl chain that is esteror ether-bound to a polar head group such as phosphoglycerol, or a glycerol that is glycosidically bound to a sugar moiety They are major components of phytoplankton biomass [12, 13], of which the less labile fraction survives degradation in the water column [14] and is degraded by microorganisms in the underlying sediments [15]. Longchain fatty acids released from lipid hydrolysis are energyrich compounds [16], and can be expected to be favorable substrates for microorganisms

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