Enigmatic marine microbes share resources to overcome energy stress in the oxygen-starved ocean

Canadian and US researchers have mapped the single-cell genomes of a diverse group of microbial dark matter known as Marinimicrobia identifying previously uncharted metabolic roles, including as a potential greenhouse gas sink.

The genomes, presented in Nature Communications, provide the most detailed information on how different Marinimicrobia groups interact with other microbes to complete key metabolic processes, contributing to important marine ecosystem services.

“Marinimicrobia are essential but enigmatic members of marine microbial communities adapted to thrive under low oxygen conditions,” said co-author and University of British Columbia (UBC) researcher Steven Hallam.

“They do this by forming partnerships with other microbes that overcome energy stress and promote dynamic mutualism.”

Dissolved oxygen concentration is an important organizing principle in marine ecosystems because it determines how much energy is available for growth of single- and multi-cellular life forms. As oxygen levels decline, energy is increasingly routed into microbial metabolism. That in turn can lead to nitrogen loss and the production of greenhouse gases like nitrous oxide and methane.

The newly discovered roles displayed by some groups of Marinimicrobia appear to counter that process.

“The energy metabolism of Marinimicrobia plays significant roles in global nitrogen and sulfur cycling,” said lead-author Alyse Hawley, a UBC microbiologist. “Our findings indicate the potential for some Marinimicrobia groups to act as biological filters for the potent greenhouse gas nitrous oxide, a previously unrecognized niche in the ocean.”

The study brings together research groups at UBC, University of Illinois, Bigelow Laboratory for Ocean Sciences and the Joint Genome Institute (JGI), a DOE Office of Science User Facility at Lawrence Berkeley National Laboratory. The work combines cutting edge sequencing and analysis methods with time series observations to chart microbial interactions.

“By directing our expertise in single-cell genomics through the JGI’s Community Science Program, we contributed the first genomic insights into the candidate phylum Marinimicrobia,” said co-author Tanja Woyke, JGI Microbial Genomics Program Head.

“The study took these data one step further by applying a more expansive omics toolkit that included metagenomics and metatanscriptomics – profiling of community-wide gene expression – to study Marinimicrobia along defined energy gradients. This work beautifully illustrates how evolutionary diversification within the Marinimicrobia dark matter lineage can lead to adaptation to different energetic niches and ultimately their occupation.”

Building on this observation, Ramunas Stepanauskas, Director of the Single Cell Genomics Center (SCGC) at the Bigelow Laboratory for Ocean Sciences and co-author said: “This work demonstrates the increasing capacity of molecular, cultivation-independent tools to decipher complex biogeochemical processes and microbial interactions in nature.”

The researchers used single-cell Marinimicrobia genomes collected from multiple oceanic locales as platforms to recruit environmental DNA and RNA sequences enabling robust reconstruction of Marinimicrobia metabolism under different oxygen concentrations.

Oxygen starvation can negatively impact ecosystem services through changes in food web structure and reduced biological diversity. Currently, oxygen starved regions of the ocean called oxygen minimum zones (OMZs) constitute up to seven per cent of global ocean volume. Ongoing changes in ocean water temperature and circulation patterns are resulting in OMZ expansion. 

Continued expansion of OMZs has the potential to transport oxygen-depleted waters into coastal regions, adversely effecting fisheries and impacting the balance of greenhouse gases in the atmosphere.

“When viewed from a socio-economic perspective, these observations take on immediate significance as we consider how energy stress can promote metabolic cooperation in the microbial world,” said Hallam. “By emulating these strategies in our own approach to energy and materials production, human beings might be in a much more tenable position to support sustainable growth.”