Metabolic flexibility allows generalist bacteria to become dominant in a frequently disturbed ecosystem

Chen, Ya-Jou; Leung, Pok Man; Bay, Sean K.; Hugenholtz, Philip; Kessler, Adam J.; Shelley, Guy; Waite, David W.; Cook, Perran; Greening, Chris

doi:10.1101/2020.02.12.945220

Cited by 20 publications

(19 citation statements)

References 82 publications

(86 reference statements)

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“…This is in line with previous studies that showed Woeseiales is an abundant lineage in marine sediments worldwide [7,12,13], although the properties that determine such ecological success are poorly understood. Previous work has suggested metabolic plasticity to be at the root of the global distribution and high abundance continuously observed for Woeseiales worldwide [7,13,15]. Our high-resolution transcriptional evidence supports this idea and suggests that the Woeseiales in these Arctic fjords are able to sense and adapt to their environment upon burial, most likely in response to changes in redox chemistry.…”

Section: Discussionsupporting

confidence: 85%

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Woeseiales transcriptional response to shallow burial in Arctic fjord surface sediment

Buongiorno

Sipes²,

Wasmund³

et al. 2020

PLoS ONE

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Distinct lineages of Gammaproteobacteria clade Woeseiales are globally distributed in marine sediments, based on metagenomic and 16S rRNA gene analysis. Yet little is known about why they are dominant or their ecological role in Arctic fjord sediments, where glacial retreat is rapidly imposing change. This study combined 16S rRNA gene analysis, metagenome-assembled genomes (MAGs), and genome-resolved metatranscriptomics uncovered the in situ abundance and transcriptional activity of Woeseiales with burial in four shallow sediment sites of Kongsfjorden and Van Keulenfjorden of Svalbard (79˚N). We present five novel Woeseiales MAGs and show transcriptional evidence for metabolic plasticity during burial, including sulfur oxidation with reverse dissimilatory sulfite reductase (dsrAB) down to 4 cm depth and nitrite reduction down to 6 cm depth. A single stress protein, spore protein SP21 (hspA), had a tenfold higher mRNA abundance than any other transcript, and was a hundredfold higher on average than other transcripts. At three out of the four sites, SP21 transcript abundance increased with depth, while total mRNA abundance and richness decreased, indicating a shift in investment from metabolism and other cellular processes to build-up of spore protein SP21. The SP21 gene in MAGs was often flanked by genes involved in membrane-associated stress response. The ability of Woeseiales to shift from sulfur oxidation to nitrite reduction with burial into marine sediments with decreasing access to overlying oxic bottom waters, as well as enter into a dormant state dominated by SP21, may account for its ubiquity and high abundance in marine sediments worldwide, including those of the rapidly shifting Arctic.

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Section: Discussionsupporting

confidence: 85%

“…This supports the idea that different populations of Woeseiales may have fundamentally different physiologies. Even single representatives of Woesiales have been hypothesized to be metabolic generalists, with evidence for a high degree of metabolic flexibility [15].…”

Section: Introductionmentioning

confidence: 99%

Woeseiales transcriptional response to shallow burial in Arctic fjord surface sediment

Buongiorno

Sipes²,

Wasmund³

et al. 2020

PLoS ONE

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“…We did not find any mOTU encoding all the putative oxidation genes in the core genome (Figure 2 and 5). Metabolic flexibility is a key factor governing distributions of taxa across ecosystems (54). However, in this study we did not find a correlation between how widespread an mOTU is and their capacity to use different electron acceptors.…”

Section: The Metabolic Potential Of the Most Abundant Chlorobium Groupscontrasting

confidence: 79%

FreshwaterChlorobiaexhibit metabolic specialization among cosmopolitan and endemic populations

Garcia

Mehrshad

Buck

et al. 2020

Preprint

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Photosynthetic bacteria from the class Chlorobia (formerly phylum Chlorobi) sustain carbon fixation in anoxic water columns. They harvest light at extremely low intensities and use various inorganic electron donors to fix carbon dioxide into biomass. Until now, most information on their functional ecology and local adaptations came from isolates and merely 26 sequenced genomes that are poor representatives of natural populations. To address these limitations, we analyzed global metagenomes to profile planktonic Chlorobia cells from the oxyclines of 42 freshwater bodies, spanning subarctic to tropical regions and encompassing all four seasons. We assembled and compiled over 500 genomes, including metagenome-assembled genomes (MAGs), single-cell genomes (SAGs), and reference genomes from cultures, clustering them into 71 metagenomic operational taxonomic units (mOTUs) or "species". Of the 71 mOTUs, 57 were classified as genus Chlorobium and these mOTUs varied in relative abundance up to ~60% of the microbial communities in the sampled anoxic waters. Several Chlorobium-associated mOTUs were globally distributed whereas others were endemic to individual lakes. Although most clades encoded the ability to oxidize hydrogen, many were lacking genes for the oxidation of specific sulfur and iron substrates. Surprisingly, one globally distributed Scandinavian Chlorobium clade encoded the ability to oxidize hydrogen, sulfur, and iron, suggesting that metabolic versatility facilitated such widespread colonization. Overall, these findings provide new insights into the biogeography of the Chlorobia and the metabolic traits that facilitate niche specialization within lake ecosystems.

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“…This agrees with recent reports that environmental and spatial drivers differentially act on common and rare taxa ( 77 , 78 ). Abundant generalists and rare specialists have been shown to differentially respond to environmental change, reflecting differences in niche breadth ( 11 , 79 , 80 ). Beyond these pairwise observations, we used zeta diversity to demonstrate that the turnover patterns reflect those typically observed in deterministically structured communities.…”

Section: Discussionmentioning

confidence: 99%

Soil Bacterial Communities Exhibit Strong Biogeographic Patterns at Fine Taxonomic Resolution

et al. 2020

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Bacteria have been inferred to exhibit relatively weak biogeographic patterns. To what extent such findings reflect true biological phenomena or methodological artifacts remains unclear. Here, we addressed this question by analyzing the turnover of soil bacterial communities from three data sets. We applied three methodological innovations: (i) design of a hierarchical sampling scheme to disentangle environmental from spatial factors driving turnover; (ii) resolution of 16S rRNA gene amplicon sequence variants to enable higher-resolution community profiling; and (iii) application of the new metric zeta diversity to analyze multisite turnover and drivers. At fine taxonomic resolution, rapid compositional turnover was observed across multiple spatial scales. Turnover was overwhelmingly driven by deterministic processes and influenced by the rare biosphere. The communities also exhibited strong distance decay patterns and taxon-area relationships, with z values within the interquartile range reported for macroorganisms. These biogeographical patterns were weakened upon applying two standard approaches to process community sequencing data: clustering sequences at 97% identity threshold and/or filtering the rare biosphere (sequences lower than 0.05% relative abundance). Comparable findings were made across local, regional, and global data sets and when using shotgun metagenomic markers. Altogether, these findings suggest that bacteria exhibit strong biogeographic patterns, but these signals can be obscured by methodological limitations. We advocate various innovations, including using zeta diversity, to advance the study of microbial biogeography. IMPORTANCE It is commonly thought that bacterial distributions show lower spatial variation than for multicellular organisms. In this article, we present evidence that these inferences are artifacts caused by methodological limitations. Through leveraging innovations in sampling design, sequence processing, and diversity analysis, we provide multifaceted evidence that bacterial communities in fact exhibit strong distribution patterns. This is driven by selection due to factors such as local soil characteristics. Altogether, these findings suggest that the processes underpinning diversity patterns are more unified across all domains of life than previously thought, which has broad implications for the understanding and management of soil biodiversity.

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Metabolic flexibility allows generalist bacteria to become dominant in a frequently disturbed ecosystem

Cited by 20 publications

References 82 publications

Woeseiales transcriptional response to shallow burial in Arctic fjord surface sediment

Woeseiales transcriptional response to shallow burial in Arctic fjord surface sediment

FreshwaterChlorobiaexhibit metabolic specialization among cosmopolitan and endemic populations

Soil Bacterial Communities Exhibit Strong Biogeographic Patterns at Fine Taxonomic Resolution

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