Publications

Chemosynthetic primary production by symbiotic microbes powers entire ecosystems in the remote deep sea. New research shows that in shallow waters chemosynthetic symbioses can contribute substantially to a vital economic resource - lobster fisheries in the Caribbean Sea.

Ocean microbes drive biogeochemical cycling on a global scale1. However, this cycling is constrained by viruses that affect community composition, metabolic activity, and evolutionary trajectories2, 3. Owing to challenges with the sampling and cultivation of viruses, genome-level viral diversity remains poorly described and grossly understudied, with less than 1% of observed surface-ocean viruses known4. Here we assemble complete genomes and large genomic fragments from both surface- and deep-ocean viruses sampled during the Tara Oceans and Malaspina research expeditions5, 6, and analyse the resulting ‘global ocean virome’ dataset to present a global map of abundant, double-stranded DNA viruses complete with genomic and ecological contexts. A total of 15,222 epipelagic and mesopelagic viral populations were identified, comprising 867 viral clusters (defined as approximately genus-level groups7, 8). This roughly triples the number of known ocean viral populations4 and doubles the number of candidate bacterial and archaeal virus genera8, providing a near-complete sampling of epipelagic communities at both the population and viral-cluster level. We found that 38 of the 867 viral clusters were locally or globally abundant, together accounting for nearly half of the viral populations in any global ocean virome sample. While two-thirds of these clusters represent newly described viruses lacking any cultivated representative, most could be computationally linked to dominant, ecologically relevant microbial hosts. Moreover, we identified 243 viral-encoded auxiliary metabolic genes, of which only 95 were previously known. Deeper analyses of four of these auxiliary metabolic genes (dsrC, soxYZ, P-II (also known as glnB) and amoC) revealed that abundant viruses may directly manipulate sulfur and nitrogen cycling throughout the epipelagic ocean. This viral catalog and functional analyses provide a necessary foundation for the meaningful integration of viruses into ecosystem models where they act as key players in nutrient cycling and trophic networks.

The marine subsurface sediment biosphere is widely inhabited by bacteria affiliated with the class Dehalococcoidia (DEH), phylum Chloroflexi, yet little is known regarding their metabolisms. In this report, genomic content from a single DEH cell (‘DEH-C11’) with a 16S rRNA gene that affiliated with a diverse cluster of 16S rRNA gene sequences prevalent in marine sediments, was obtained from sediments of Aarhus Bay, Denmark. The distinctive gene content of this cell suggests metabolic characteristics that differ from those of known DEH and Chloroflexi. Genes encoding dissimilatory sulfite reductase (Dsr) suggest DEH could respire oxidized sulfur compounds, although Chloroflexi have never been implicated in this mode of sulfur cycling. Using long-range PCR assays targeting DEH dsr-loci, dsrAB were amplified and sequenced from various marine sediments. Many of the amplified dsrAB sequences affiliated with the DEH Dsr-clade, which we propose equates to a family-level clade. This provides supporting evidence for the potential for sulfite reduction by diverse DEH. DEH-C11 also harboured genes encoding reductases for arsenate, dimethyl sulfoxide and halogenated organics. The reductive dehalogenase homolog (RdhA) forms a monophyletic clade along with RdhA sequences from various DEH-derived contigs retrieved from available metagenomes. Multiple facts indicate this RdhA may not be a terminal reductase. Other genes indicated nutrients and energy may be derived from the oxidation of substituted homocyclic and heterocyclic aromatic compounds. Together, these results suggest that marine DEH play a previously unrecognised role in sulfur cycling, and reveal potential for expanded catabolic and respiratory functions among subsurface DEH.

Rice paddies are indispensable for human food supply but emit large amounts of the greenhouse gas methane. Sulfur cycling occurs at high rates in these water-submerged soils and controls methane production, an effect that is increased by sulfate-containing fertilizers or soil amendments. We grew rice plants until their late vegetative phase with and without gypsum (CaSO4 ·2H2 O) amendment and identified responsive bacteria by 16S rRNA gene amplicon sequencing. Gypsum amendment decreased methane emissions by up to 99% but had no major impact on the general phylogenetic composition of the bacterial community. It rather selectively stimulated or repressed a small number of 129 and 27 species-level operational taxonomic units (OTUs) (out of 1,883-2,287 observed) in the rhizosphere and bulk soil, respectively. Gypsum-stimulated OTUs were affiliated with several potential sulfate-reducing (Syntrophobacter, Desulfovibrio, unclassified Desulfobulbaceae, unclassified Desulfobacteraceae) and sulfur-oxidizing taxa (Thiobacillus, unclassified Rhodocyclaceae), while gypsum-repressed OTUs were dominated by aerobic methanotrophs (Methylococcaceae). Abundance correlation networks suggested that two abundant (>1%) OTUs (Desulfobulbaceae, Rhodocyclaceae) were central to the reductive and oxidative parts of the sulfur cycle.

Microorganisms are vital in mediating the earth's biogeochemical cycles; yet, despite our rapidly increasing ability to explore complex environmental microbial communities, the relationship between microbial community structure and ecosystem processes remains poorly understood. Here, we address a fundamental and unanswered question in microbial ecology: 'When do we need to understand microbial community structure to accurately predict function?' We present a statistical analysis investigating the value of environmental data and microbial community structure independently and in combination for explaining rates of carbon and nitrogen cycling processes within 82 global datasets. Environmental variables were the strongest predictors of process rates but left 44% of variation unexplained on average, suggesting the potential for microbial data to increase model accuracy. Although only 29% of our datasets were significantly improved by adding information on microbial community structure, we observed improvement in models of processes mediated by narrow phylogenetic guilds via functional gene data, and conversely, improvement in models of facultative microbial processes via community diversity metrics. Our results also suggest that microbial diversity can strengthen predictions of respiration rates beyond microbial biomass parameters, as 53% of models were improved by incorporating both sets of predictors compared to 35% by microbial biomass alone. Our analysis represents the first comprehensive analysis of research examining links between microbial community structure and ecosystem function. Taken together, our results indicate that a greater understanding of microbial communities informed by ecological principles may enhance our ability to predict ecosystem process rates relative to assessments based on environmental variables and microbial physiology.

Dissimilatory sulfate reduction in peatlands is sustained by a cryptic sulfur cycle and effectively competes with methanogenic degradation pathways. In a series of peat soil microcosms incubated over 50 days, we identified bacterial consortia that responded to small, periodic additions of individual fermentation products (formate, acetate, propionate, lactate or butyrate) in the presence or absence of sulfate. Under sulfate supplementation, net sulfate turnover (ST) steadily increased to 16-174 nmol cm-3 per day and almost completely blocked methanogenesis. 16S rRNA gene and cDNA amplicon sequencing identified microorganisms whose increases in ribosome numbers strongly correlated to ST. Natively abundant (⩾0.1% estimated genome abundance) species-level operational taxonomic units (OTUs) showed no significant response to sulfate. In contrast, low-abundance OTUs responded significantly to sulfate in incubations with propionate, lactate and butyrate. These OTUs included members of recognized sulfate-reducing taxa (Desulfosporosinus, Desulfopila, Desulfomonile, Desulfovibrio) and also members of taxa that are either yet unknown sulfate reducers or metabolic interaction partners thereof. Most responsive OTUs markedly increased their ribosome content but only weakly increased in abundance. Responsive Desulfosporosinus OTUs even maintained a constantly low population size throughout 50 days, which suggests a novel strategy of rare biosphere members to display activity. Interestingly, two OTUs of the non-sulfate-reducing genus Telmatospirillum (Alphaproteobacteria) showed strongly contrasting preferences towards sulfate in butyrate-amended microcosms, corroborating that closely related microorganisms are not necessarily ecologically coherent. We show that diverse consortia of low-abundance microorganisms can perform peat soil sulfate reduction, a process that exerts control on methane production in these climate-relevant ecosystems.

Genes encoding dissimilatory sulfite reductase (DsrAB) are commonly used as diagnostic markers in ecological studies of sulfite- and sulfate-reducing microorganisms. Here, we developed new high-coverage primer sets for generation of reductive bacterial-type dsrA and dsrB PCR products for highly parallel amplicon sequencing and a bioinformatics workflow for processing and taxonomic classification of short dsrA and dsrB reads. We employed two diverse mock communities that consisted of 45 or 90 known dsrAB sequences derived from environmental clones to precisely evaluate the performance of individual steps of our amplicon sequencing approach on the Illumina MiSeq platform. Although PCR cycle number, gene-specific primer mismatches, and stringent filtering for high-quality sequences had notable effects on the observed dsrA and dsrB community structures, recovery of most mock community sequences was generally proportional to their relative input abundances. Successful dsrA and dsrB diversity analysis in selected environmental samples further proved that the multiplex amplicon sequencing approach is adequate for monitoring spatial distribution and temporal abundance dynamics of dsrAB-containing microorganisms. While tested for reductive bacterial-type dsrAB, this method is readily applicable for oxidative-type dsrAB of sulfur-oxidizing bacteria and also provides guidance for processing short amplicon reads of other functional genes.