Streamlined and Abundant Bacterioplankton Thrive in Functional Cohorts

Mondav, Rhiannon; Bertilsson, Stefan; Buck, Moritz; Langenheder, Silke; Lindström, Eva S.; Garcia, Sarahi L.

doi:10.1128/msystems.00316-20

Cited by 14 publications

(16 citation statements)

References 86 publications

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“…While further investigating this unsolved discrepancy, we discovered that all genomes of the acI lineage were deficient in the heme biosynthetic pathway ( Extended Data Fig. 1 ; discussed in more detail below), which was also reported in a recent study 15 . This finding led us to speculate that acI bacteria require heme, an essential cofactor of catalase, for their growth, rather than the H 2 O 2 scavenging function of catalase.…”

Section: Figsupporting

confidence: 72%

Heme auxotrophy in abundant aquatic microbial lineages

Kim

Kang

Lee

et al. 2021

Preprint

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Heme, a porphyrin ring complexed with iron, is a metalloprosthetic group of numerous proteins involved in diverse metabolic and respiratory processes across all domains of life, and is thus considered essential for respiring organisms1,2. Several microbial groups are known to lack the de novo heme biosynthetic pathway and therefore require exogenous heme from the environment3. These heme auxotroph groups are largely limited to pathogens4,5, symbionts6,7, or microorganisms living in nutrient-replete conditions8, whereas the complete absence of heme biosynthesis is extremely rare in free-living organisms9. Here, we show that the acI lineage, a predominant and ubiquitous free-living bacterial group in freshwater habitats, is auxotrophic for heme. We found that two recently cultivated acI isolates10 require exogenous heme for their growth. According to whole-genome analyses, all (n=20) isolated acI strains lacked essential enzymes necessary for heme biosynthesis, indicating that heme auxotrophy is a conserved trait in this lineage. Analyses of >24,000 representative genomes for species clusters of the Genome Taxonomy Database (GTDB) revealed that heme auxotrophy is widespread across abundant but not-yet-cultivated microbial groups, including Patescibacteria, Marinisomatota (SAR406), Actinomarinales (OM1), and marine group III Euryarchaeota. Our findings indicate that heme auxotrophy is a more common phenomenon than previously thought, and may lead to use of heme as a growth factor to increase the cultured microbial diversity.

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Section: Figsupporting

confidence: 72%

Heme auxotrophy in abundant aquatic microbial lineages

Kim

Kang

Lee

et al. 2021

Preprint

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“…For a complete list of archaeal phyla please see Figure 3. Fusobacteriota (94) Deinococcota (93) Thermotogota (83) Fibrobacterota (82) Eremiobacterota (75) Synergistota (64) Dependentiae (58) Binatota (57) Chloroflexota_A (52…”

Section: Resultsmentioning

confidence: 99%

“…Aquatic microorganisms have been used as exemplary cases of streamlining in which many have gone through community adaptive selections and gene loss (56). In fact, their gene loss goes so far that these free-living aquatic microorganisms depend on community associations and thus thrive in functional cohorts (57). The renewed view of genome sizes and characteristics confirms that genomes from aquatic microorganisms have a higher coding density compared to those from other ecosystems ( Figure 1).…”

Section: Extant Genome Size Distribution In the Environmentmentioning

confidence: 88%

“…Their gene loss goes so far that they become auxotrophic, meaning they cannot biosynthesize essential metabolites. One strategy to overcome their required nutritional needs is to thrive in functional cohorts (52). As opposed to prototrophic lifestyle, auxotrophic lifestyle is reflected by smaller genome sizes (25, 41, 53, 54) (Table S1).…”

Section: Impact Of Ecosystem and Trophic Strategy On Genome Sizementioning

confidence: 99%

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A genomic perspective across Earth’s microbiomes reveals that genome size in Archaea and Bacteria is linked to ecosystem type and trophic strategy

Rodríguez-Gijón

Nuy

Mehrshad

et al. 2021

Preprint

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Our view of genome size distribution in Bacteria and Archaea has remained skewed as the data used to paint its picture has been dominated by genomes of microorganisms that can be cultivated under laboratory settings. However, the continuous effort to catalogue the genetic make-up of Earth’s microbiomes, specifically propelled by recent extensive work on uncultivated microorganisms, provides a unique opportunity to revise our perspective on genome size distribution. Genome size is largely a function of the expansion and contraction, by gain or loss of DNA elements. While genome expansion provides microorganisms the capability to acquire a wide repertoire of ecological functions, genome reduction increases the fitness of the microorganisms to very specific niches. Capitalizing on a recently released large catalog of tens of thousands of metagenome-assembled genomes, we here provide a comprehensive overview of genome size distributions, suggesting that the known phylogenetic diversity of environmental microorganisms possess significantly smaller genomes (aquatic bacteria average 3.1 Mb, host-associated bacterial genomes average 3.0 Mb, and terrestrial bacteria average 3.8 Mb) than the collection of laboratory isolated microorganisms (average 4.4 Mb). Moreover, the variation in genome sizes across different types of environments reflects the different ecological and evolutionary strategies used by microorganisms to thrive in their native environment. Finally, the fact that genome sizes in Bacteria and Archaea remain relatively small might be a reflection of the constraints imposed by selection and an overall dominance of gene loss as a survival strategy.

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“…These so-called model communities are a powerful way to study the microbial interaction in a semi-natural environment (10). Model communities also provide tools for building hypotheses that could then be further tested by looking into interaction networks in time series of natural environments (11).…”

Section: Introductionmentioning

confidence: 99%

Biogenic methane cycling is controlled by microbial cohorts

Mondav

Martin

Peura

et al. 2022

Preprint

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The generation and consumption of methane by aquatic microbial communities is an important contribution to the global carbon budget. We sought to broaden understanding of consortia members and interactions by combining multiple methods including analysis of natural and cultivated microbial communities. By analysing the microbial community composition and co-occurrence patterns of a lake time-series we were able to identify potential consortia involved in methane cycling. In combination with methane flux, we also analysed the community composition and co-occurrence patterns of reduced microbial model communities with inoculum from the same lake. While the network analyses confirmed many known associations, when combined with results from mixed cultures, we noted new players in methane cycling. Cultivated model communities were shown to be an effective method to explore the rarer but still important players in methane cycling and for identifying new putative members. Here we show that using multiple methods to approach the complex problem of methane cycling consortia yields not just insights into the known taxa but highlights potential new members creating new hypotheses to be tested.

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Streamlined and Abundant Bacterioplankton Thrive in Functional Cohorts

Cited by 14 publications

References 86 publications

Heme auxotrophy in abundant aquatic microbial lineages

Heme auxotrophy in abundant aquatic microbial lineages

A genomic perspective across Earth’s microbiomes reveals that genome size in Archaea and Bacteria is linked to ecosystem type and trophic strategy

Biogenic methane cycling is controlled by microbial cohorts

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