Lifestyles of rarity: understanding heterotrophic strategies to inform the ecology of the microbial rare biosphere

Newton, Ryan J.; Shade, Ashley

doi:10.3354/ame01801

Cited by 39 publications

(40 citation statements)

References 100 publications

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“…However, even taxa that increased in abundance did not show fluctuations over the sampling days, regardless if they were subjected to pulse‐ or press‐disturbances. This indicates that rare taxa might not be opportunistic and therefore subject to sudden blooms and subsequent decline as has been suggested in previous studies (Newton and Shade, ). However, the time period of observation might have been too short to detect such a decline.…”

Section: Discussionsupporting

confidence: 73%

A low proportion of rare bacterial taxa responds to abiotic changes compared with dominant taxa

Kurm

Geisen

Hol

2018

Environmental Microbiology

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Summary In many studies, rare bacterial taxa have been found to increase in response to environmental changes. These changes have been proposed to contribute to the insurance of ecosystem functions. However, it has not been systematically tested if rare taxa are more likely to increase in abundance than dominant taxa. Here, we study whether rare soil bacterial taxa are more likely to respond to environmental disturbances and if rare taxa are more opportunistic than dominant taxa. To test this, we applied nine different disturbance treatments to a grassland soil and observed changes in bacterial community composition over 7 days. While 12% of the dominant taxa changed in abundance, only 1% of the rare taxa showed any effect. Rare taxa increased in response to a single disturbance treatment only, while dominant taxa responded to up to five treatments. We conclude that rare taxa are not more likely to contribute to community dynamics after disturbances than dominant taxa. Nevertheless, as rare taxa outnumber abundant taxa with here 230 taxa that changed significantly, the chance is high that some of these rare taxa might act as ecologically important keystone taxa. Therefore, rare and abundant taxa might both contribute to ecosystem insurance.

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Section: Discussionsupporting

confidence: 73%

A low proportion of rare bacterial taxa responds to abiotic changes compared with dominant taxa

Kurm

Geisen

Hol

2018

Environmental Microbiology

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“…Compared to macroorganisms, delineating spatial distribution areas in microorganisms is much more challenging, as well as inferring life strategies (e.g., habitat generalist/specialist, copiotrophs/oligotrophs, Newton and Shade ()) from those spatial patterns. First, how microbes perceive their environment at the microscale remains poorly understood (Stocker, ), and we do not even have an accurate estimate of the total microbial diversity present in a sample (Locey & Lennon, ).…”

Section: Discussionmentioning

confidence: 99%

Higher contribution of globally rare bacterial taxa reflects environmental transitions across the surface ocean

et al. 2019

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Microbial taxa range from being ubiquitous and abundant across space to extremely rare and endemic, depending on their ecophysiology and on different processes acting locally or regionally. However, little is known about how cosmopolitan or rare taxa combine to constitute communities and whether environmental variations promote changes in their relative abundances. Here we identified the Spatial Abundance Distribution (SpAD) of individual prokaryotic taxa (16S rDNA‐defined Operational Taxonomic Units, OTUs) across 108 globally‐distributed surface ocean stations. We grouped taxa based on their SpAD shape (“normal‐like”‐ abundant and ubiquitous; “logistic”‐ globally rare, present in few sites; and “bimodal”‐ abundant only in certain oceanic regions), and investigated how the abundance of these three categories relates to environmental gradients. Most surface assemblages were numerically dominated by a few cosmopolitan “normal‐like” OTUs, yet there was a gradual shift towards assemblages dominated by “logistic” taxa in specific areas with productivity and temperature differing the most from the average conditions in the sampled stations. When we performed the SpAD categorization including additional habitats (deeper layers and particles of varying sizes), the SpAD of many OTUs changed towards fewer “normal‐like” shapes, and OTUs categorized as globally rare in the surface ocean became abundant. This suggests that understanding the mechanisms behind microbial rarity and dominance requires expanding the context of study beyond local communities and single habitats. We show that marine bacterial communities comprise taxa displaying a continuum of SpADs, and that variations in their abundances can be linked to habitat transitions or barriers that delimit the distribution of community members.

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“…Increased rates and spectra of enzyme activities characterized amended mesocosms from all locations (Figs and , Supporting Information Figs S7 and S8) and co‐occurred with the predominance of initially rare taxa within specific families of the Gammproteobacteria , Alphaproteobacteria and Flavobacteria (Supporting Information Figs S3–S5). Many of these bacteria are presumably copiotrophic, conditionally rare taxa (Shade et al, ) and possess genetic repertoires – including a wider range of extracellular enzymes (Lauro et al, ) – that enable rapid exploitation of pulses of organic matter (Newton and Shade, ). The boom and bust patterns of these taxa in our amended mesocosms are congruent with temporal succession patterns exhibited by conditionally rare copiotrophs (Shade et al, ; Alonso‐Sáez et al, ; Newton and Shade, ).…”

Section: Discussionmentioning

confidence: 99%

“…Many of these bacteria are presumably copiotrophic, conditionally rare taxa (Shade et al, 2014) and possess genetic repertoiresincluding a wider range of extracellular enzymes (Lauro et al, 2009)that enable rapid exploitation of pulses of organic matter (Newton and Shade, 2016). The boom and bust patterns of these taxa in our amended mesocosms are congruent with temporal succession patterns exhibited by conditionally rare copiotrophs (Shade et al, 2014;Alonso-Sáez et al, 2015;Newton and Shade, 2016). Given their dominance in amended mesocosms, these conditional members of the rare biosphere (Sogin et al, 2006) likely play a major role in the degradation of sporadically available HMW-OM.…”

Section: Conditionally Rare Taxa Drive Convergent Features Of Composimentioning

confidence: 99%

Community structural differences shape microbial responses to high molecular weight organic matter

Balmonte

Buckley

Hoarfrost

et al. 2018

Environmental Microbiology

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Summary The extent to which differences in microbial community structure result in variations in organic matter (OM) degradation is not well understood. Here, we tested the hypothesis that distinct marine microbial communities from North Atlantic surface and bottom waters would exhibit varying compositional succession and functional shifts in response to the same pool of complex high molecular weight (HMW‐OM). We also hypothesized that microbial communities would produce a broader spectrum of enzymes upon exposure to HMW‐OM, indicating a greater potential to degrade these compounds than reflected by initial enzymatic activities. Our results show that community succession in amended mesocosms was congruent with cell growth, increased bacterial production and most notably, with substantial shifts in enzymatic activities. In all amended mesocosms, closely related taxa that were initially rare became dominant at time frames during which a broader spectrum of active enzymes were detected compared to initial timepoints, indicating a similar response among different communities. However, succession on the whole‐community level, and the rates, spectra and progression of enzymatic activities, reveal robust differences among distinct communities from discrete water masses. These results underscore the crucial role of rare bacterial taxa in ocean carbon cycling and the importance of bacterial community structure for HMW‐OM degradation.

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Lifestyles of rarity: understanding heterotrophic strategies to inform the ecology of the microbial rare biosphere

Cited by 39 publications

References 100 publications

A low proportion of rare bacterial taxa responds to abiotic changes compared with dominant taxa

A low proportion of rare bacterial taxa responds to abiotic changes compared with dominant taxa

Higher contribution of globally rare bacterial taxa reflects environmental transitions across the surface ocean

Community structural differences shape microbial responses to high molecular weight organic matter

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