Diel changes in bacteriochlorophyll a concentration suggest rapid bacterioplankton cycling in the Baltic Sea

Koblížek, Michal; Stoń-Egiert, Joanna; Sagan, Sławomir; Kolber, Zbigniew

doi:10.1016/j.femsec.2004.09.016

Cited by 51 publications

(17 citation statements)

References 32 publications

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“…Consequently, generalizing statements postulating a stringent inhibition of BChl synthesis in marine aerobic anoxygenic photosynthetic bacteria even by low light intensities [ e.g. 36], [37] have to be reconsidered. Interestingly, our data are in line with early results of Kolber et al [38] who found only a minor effect of light on pigment synthesis in aerobic bacteriochlorophyll-containing bacteria in marine ecosystems, but a diel growth cycle in oxygenic phototrophs with chlorophyll synthesis restricted to periods of darkness.…”

Section: Resultsmentioning

confidence: 99%

The Photosynthetic Apparatus and Its Regulation in the Aerobic Gammaproteobacterium Congregibacter litoralis gen. nov., sp. nov

et al. 2009

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BackgroundThere is accumulating evidence that in some marine environments aerobic bacteriochlorophyll a-producing bacteria represent a significant part of the microbial population. The interaction of photosynthesis and carbon metabolism in these interesting bacteria is still largely unknown and requires further investigation in order to estimate their contribution to the marine carbon cycle.Methodology/Principal FindingsHere, we analyzed the structure, composition and regulation of the photosynthetic apparatus in the obligately aerobic marine gammaproteobacterium KT71T. Photoheterotrophically grown cells were characterized by a poorly developed lamellar intracytoplasmic membrane system, a type 1 light-harvesting antenna complex and a photosynthetic reaction center associated with a tetraheme cytochrome c. The only photosynthetic pigments produced were bacteriochlorophyll a and spirilloxanthin. Under semiaerobic conditions KT71T cells expressing a photosynthetic apparatus showed a light-dependent increase of growth yield in the range of 1.3–2.5 fold. The expression level of the photosynthetic apparatus depended largely on the utilized substrate, the intermediary carbon metabolism and oxygen tension. In addition, pigment synthesis was strongly influenced by light, with blue light exerting the most significant effect, implicating that proteins containing a BLUF domain may be involved in regulation of the photosynthetic apparatus. Several phenotypic traits in KT71T could be identified that correlated with the assumed redox state of growing cells and thus could be used to monitor the cellular redox state under various incubation conditions.Conclusions/SignificanceIn a hypothetical model that explains the regulation of the photosynthetic apparatus in strain KT71T we propose that the expression of photosynthesis genes depends on the cellular redox state and is maximal under conditions that allow a balanced membrane redox state. So far, bacteria capable of an obligately aerobic, photosynthetic metabolism constitute a unique phenotype within the class Gammaproteobacteria, so that it is justified to propose a new genus and species, Congregibacter litoralis gen. nov, sp. nov., represented by the type strain KT71T ( = DSM 17192T = NBRC 104960T).

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Section: Resultsmentioning

confidence: 99%

The Photosynthetic Apparatus and Its Regulation in the Aerobic Gammaproteobacterium Congregibacter litoralis gen. nov., sp. nov

et al. 2009

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“…where t is time, D is the decay rate, [BChl a] t is BChl a signal at time t, and [BChl a] start is the initial BChl a signal recorded in the morning (Koblížek et al 2005).…”

Section: Bacteriochlorophyll Turnover Measurementsmentioning

confidence: 99%

“…This pigment is found in aerobic anoxygenic phototrophic (AAP) bacteria (i.e., photoheterotrophic organisms), which represented 1-4% of the total bacteria in the studied regions (Koblížek 2015). Diel changes of this pigment were earlier proposed as a convenient way to determine the mortality of AAP bacteria (Koblížek et al 2005), which is related to the growth rate under steady-state conditions (Koblížek et al 2007). We conducted BChl a turnover rate measurements during BIOSOPE, OC443, and KM1013.…”

Section: Independent Corroboration Of Rapid Membrane Turnover Ratesmentioning

confidence: 99%

Phospholipid turnover rates suggest that bacterial community growth rates in the open ocean are systematically underestimated

Popendorf

Koblížek

Mooy

2020

Limnology & Oceanography

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Heterotrophic bacteria in the surface ocean play a critical role in the global carbon cycle and the magnitude of this role depends on their growth rates. Although methods for determining bacterial community growth rates based on incorporation of radiolabeled thymidine and leucine are widely accepted, they are based on a number of assumptions and simplifications. We sought to independently assess these methods by comparing bacterial growth rates to turnover rates of bacterial membranes using previously published methods in a range of openocean settings. We found that turnover rates for heterotrophic bacterial phospholipids averaged 0.80 AE 0.35 d −1. This was supported by independent measurements of turnover rates of a membrane-bound pigment in photoheterotrophic bacteria, bacteriochlorophyll a (0.85 AE 0.09 d −1). By contrast, bacterial growth rates measured by uptake of radiolabeled thymidine and leucine were 0.12 AE 0.08 d −1 , well within the range expected from the literature. We explored whether the discrepancies between phospholipid turnover rates and bacterial growth rate could be explained by membrane recycling/remodeling and other factors, but were left to conclude that the radiolabeled thymidine and leucine incorporation methods substantially underestimated actual bacterial growth rates. We use a simple model to show that the faster bacterial growth rates we observed can be accommodated within the constraints of the microbial carbon budget if bacteria are smaller than currently thought, grow with greater efficiency, or some combination of these two factors.

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Section: Response Parameters -Sampling and Analysismentioning

confidence: 99%

“…Bacteriochlorophyll a (BChl a) concentrations were measured on an FL3500-FT fluorometer (Photon Systems Instruments), using the standard calibration curve provided by the manufacturer. Samples were first treated with 3-(3, 4-dichlorophenyl)-1,1-dimethylurea (DCMU, 50 µM final concentration), an inhibitor of photosystem II in oxygenic phototrophs, so that BChl a fluorescence could be distinguished from Chl a fluorescence (Koblízek et al 2005).Samples for the microscopic enumeration of total bacterial and AAP cells were fixed immediately after collection with 1% glutaraldehyde (final concentration) and kept refrigerated in the dark until filtration. In the lab, samples were filtered onto 0.2 µm poresize black polycarbonate filters and immediately stored at −80°C.…”

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confidence: 99%

Major contribution of both zooplankton and protists to the top-down regulation of freshwater aerobic anoxygenic phototrophic bacteria

Chaves¹,

Cottrell²,

Kirchman³

et al. 2015

Aquat. Microb. Ecol.

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Aerobic anoxygenic phototrophic (AAP) bacteria are photoheterotrophic prokaryotes that use light as a secondary energy source to complement the consumption of organic matter. Despite this metabolic flexibility and their widespread distribution, their low relative abundances suggest that they may be subjected to strong regulatory processes. However, there is still little information on the regulation of AAP abundance, particularly in freshwaters. Here, we used a lake mesocosm experiment to address the top-down regulation of freshwater AAP by protists and zooplankton under 2 contrasting nutrient regimes. Our results support the hypothesis that freshwater AAP are subject to intense top-down regulation, and are selectively removed by grazers. The average gross growth rate of AAP was ca. 1.5 times higher, and grazing loss rates 1.6 times higher than those of the bulk bacterial community. Our results further indicate that whereas protists are the main predators of AAP, zooplankton may account for over a third of AAP losses, and both exhibit a greater selectivity for AAP relative to total bacteria. The mechanistic underpinning of this selectivity is still unclear, but it may be related to the average larger cell size of AAP, and to their higher potential growth rates relative to the bulk bacterial community. Our results further suggest that AAP may play a disproportionate role in the nutrition of lake zooplankton, and in the trophic transfer of organic carbon in lake food webs.KEY WORDS: Aerobic anoxygenic phototrophic bacteria · Grazing loss rate · Selective predation · Photoheterotrophy · Freshwater Resale or republication not permitted without written consent of the publisher FREE REE ACCESS CCESSContribution to AME Special 5 'SAME 13: progress and perspectives in aquatic microbial ecology ' Aquat Microb Ecol 76: 71-83, 2015 Lamy et al. , Mašín et al. 2012, Fauteux et al. 2015. Two possible hypotheses may explain their low in situ abundances: either light-derived energy has little effect on the growth and competitiveness of AAP, or, if there is an effect, there are other factors, unrelated to phototrophy, that may limit the ecological success of AAP bacteria more than that of other bacterial groups. Experimental evidence from marine environments suggests that AAP bacteria may have higher growth rates than the average bacteria (Koblízek et al. 2007, and therefore their generally low abundance should be due to high losses, either via grazing or viral infection. Indeed, the only study so far to have explored the different controls of the abundance of this group showed that protist grazing was the main regulator of the abundance of marine AAP bacteria . Beyond this marine study, however, there is still little information on the regulation of AAP abundance and activity, especially for inland waters, despite the fact that these photoheterotrophic mic robes have also been shown to be widespread in freshwater planktonic food webs (Mašín et al. 2008, Medová et al. 2011, Mašín et al. 2012, Cuperová et al. 2013,...

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Diel changes in bacteriochlorophyll a concentration suggest rapid bacterioplankton cycling in the Baltic Sea

Cited by 51 publications

References 32 publications

The Photosynthetic Apparatus and Its Regulation in the Aerobic Gammaproteobacterium Congregibacter litoralis gen. nov., sp. nov

The Photosynthetic Apparatus and Its Regulation in the Aerobic Gammaproteobacterium Congregibacter litoralis gen. nov., sp. nov

Phospholipid turnover rates suggest that bacterial community growth rates in the open ocean are systematically underestimated

Major contribution of both zooplankton and protists to the top-down regulation of freshwater aerobic anoxygenic phototrophic bacteria

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