scholarly journals Microbial Diversity of Co-occurring Heterotrophs in Cultures of Marine Picocyanobacteria

2020 ◽  
Author(s):  
Sean Michael Kearney ◽  
Elaina Thomas ◽  
Allison Coe ◽  
Sallie W. Chisholm

Abstract BackgroundProchlorococcus and Synechococcus are responsible for around 10% of global net primary productivity, serving as part of the foundation of marine food webs. Heterotrophic bacteria are often co-isolated with these picocyanobacteria in seawater enrichment cultures that contain no added organic carbon; heterotrophs grow on organic carbon supplied by the photolithoautotrophs. We have maintained these cultures of Prochlorococcus and Synechococcus for 100s to 1000s of generations; they represent ideal microcosms for examining the selective pressures shaping autotroph/heterotroph interactions. ResultsWe examine the diversity of heterotrophs in 74 enrichment cultures of these picocyanobacteria obtained from diverse areas of the global oceans. Heterotroph community composition differed between clades and ecotypes of the autotrophic ‘hosts’ but there was significant overlap in heterotroph community composition. Differences were associated with timing, location, depth, and methods of isolation, suggesting the particular conditions surrounding isolation have a persistent effect on long-term culture composition. The majority of heterotrophs in the cultures are rare in the global ocean; enrichment conditions favor the opportunistic outgrowth of these rare bacteria. We did find a few examples, such as heterotrophs in the family Rhodobacteraceae, that are ubiquitous and abundant in cultures and in the global oceans; their abundance in the wild is also positively correlated with that of picocyanobacteria. ConclusionsCollectively, the cultures converged on similar compositions, likely from bottlenecking and selection that happens during the early stages of enrichment for the picocyanobacteria. We highlight the potential for examining ecologically relevant relationships by identifying patterns of distribution of culture-enriched organisms in the global oceans.

2020 ◽  
Author(s):  
Sean Michael Kearney ◽  
Elaina Thomas ◽  
Allison Coe ◽  
Sallie W. Chisholm

Abstract BackgroundProchlorococcus and Synechococcus are responsible for around 10% of global net primary productivity, serving as part of the foundation of marine food webs. Heterotrophic bacteria are often co-isolated with these picocyanobacteria in seawater enrichment cultures that contain no added organic carbon; heterotrophs grow on organic carbon supplied by the photolithoautotrophs. We have maintained these cultures of Prochlorococcus and Synechococcus for 100s to 1000s of generations; they represent ideal microcosms for examining the selective pressures shaping autotroph/heterotroph interactions. ResultsWe examine the diversity of heterotrophs in 74 enrichment cultures of these picocyanobacteria obtained from diverse areas of the global oceans. Heterotroph community composition differed between clades and ecotypes of the autotrophic ‘hosts’ but there was significant overlap in heterotroph community composition. Differences were associated with timing, location, depth, and methods of isolation, suggesting the particular conditions surrounding isolation have a persistent effect on long-term culture composition. The majority of heterotrophs in the cultures are rare in the global ocean; enrichment conditions favor the opportunistic outgrowth of these rare bacteria. We did find a few examples, such as heterotrophs in the family Rhodobacteraceae, that are ubiquitous and abundant in cultures and in the global oceans; their abundance in the wild is also positively correlated with that of picocyanobacteria. ConclusionsCollectively, the cultures converged on similar compositions, likely from bottlenecking and selection that happens during the early stages of enrichment for the picocyanobacteria. We highlight the potential for examining ecologically relevant relationships by identifying patterns of distribution of culture-enriched organisms in the global oceans.


2021 ◽  
Vol 16 (1) ◽  
Author(s):  
Sean M. Kearney ◽  
Elaina Thomas ◽  
Allison Coe ◽  
Sallie W. Chisholm

Abstract Background The cyanobacteria Prochlorococcus and Synechococcus are responsible for around 10% of global net primary productivity, serving as part of the foundation of marine food webs. Heterotrophic bacteria are often co-isolated with these picocyanobacteria in seawater enrichment cultures that contain no added organic carbon; heterotrophs grow on organic carbon supplied by the photolithoautotrophs. For examining the selective pressures shaping autotroph/heterotroph interactions, we have made use of unialgal enrichment cultures of Prochlorococcus and Synechococcus maintained for hundreds to thousands of generations in the lab. We examine the diversity of heterotrophs in 74 enrichment cultures of these picocyanobacteria obtained from diverse areas of the global oceans. Results Heterotroph community composition differed between clades and ecotypes of the autotrophic ‘hosts’ but there was significant overlap in heterotroph community composition across these cultures. Collectively, the cultures were comprised of many shared taxa, even at the genus level. Yet, observed differences in community composition were associated with time since isolation, location, depth, and methods of isolation. The majority of heterotrophs in the cultures are rare in the global ocean, but enrichment conditions favor the opportunistic outgrowth of these rare bacteria. However, we found a few examples, such as bacteria in the family Rhodobacteraceae, of heterotrophs that were ubiquitous and abundant in cultures and in the global oceans. We found their abundance in the wild is also positively correlated with that of picocyanobacteria. Conclusions Particular conditions surrounding isolation have a persistent effect on long-term culture composition, likely from bottlenecking and selection that happen during the early stages of enrichment for the picocyanobacteria. We highlight the potential for examining ecologically relevant relationships by identifying patterns of distribution of culture-enriched organisms in the global oceans.


2020 ◽  
Author(s):  
Sean M. Kearney ◽  
Elaina Thomas ◽  
Allison Coe ◽  
Sallie W. Chisholm

ABSTRACTProchlorococcus and Synechococcus are responsible for around 10% of global net primary productivity, serving as part of the foundation of marine food webs. Heterotrophic bacteria are often co-isolated with these picocyanobacteria in seawater enrichment cultures that contain no added organic carbon; heterotrophs grow on organic carbon supplied by the photolithoautotrophs. We have maintained these cultures of Prochlorococcus and Synechococcus for 100s to 1000s of generations; they represent ideal microcosms for examining the selective pressures shaping autotroph/heterotroph interactions. Here we examine the diversity of heterotrophs in 74 enrichment cultures of these picocyanobacteria obtained from diverse areas of the global oceans. Heterotroph community composition differed between clades and ecotypes of the autotrophic ‘hosts’ but there was significant overlap in heterotroph community composition. Differences were associated with timing, location, depth, and methods of isolation, suggesting the particular conditions surrounding isolation have a persistent effect on long-term culture composition. The majority of heterotrophs in the cultures are rare in the global ocean; enrichment conditions favor the opportunistic outgrowth of these rare bacteria. We did find a few examples, such as heterotrophs in the family Rhodobacteraceae, that are ubiquitous and abundant in cultures and in the global oceans; their abundance in the wild is also positively correlated with that of picocyanobacteria. Collectively, the cultures converged on similar compositions, likely from bottlenecking and selection that happens during the early stages of enrichment for the picocyanobacteria. We highlight the potential for examining ecologically relevant relationships by identifying patterns of distribution of culture-enriched organisms in the global oceans.IMPORTANCEOne of the biggest challenges in marine microbial ecology is to begin to understand the rules that govern the self-assembly of these complex communities. The picocyanobacteria Prochlorococcus and Synechococcus comprise the most numerous photosynthetic organisms in the sea and supply a significant fraction of the organic carbon that feeds diverse heterotrophic microbes. When initially isolated into cultures, Prochlorococcus and Synechococcus carry with them select heterotrophic microorganisms that depend on them for organic carbon. The cultures self-assemble into stable communities of diverse microorganisms and are microcosms for understanding microbial interdependencies. Primarily faster-growing, relatively rare, copiotrophic heterotrophic bacteria – as opposed to oligotrophic bacteria that are abundant in picocyanobacterial habitats – are selected for in these cultures, suggesting that these copiotrophs experience these cultures as they would high carbon fluxes associated with particles, phycospheres of larger cells, or actual attachment to picocyanobacteria in the wild.


mSystems ◽  
2019 ◽  
Vol 4 (4) ◽  
Author(s):  
Barbara Bayer ◽  
Claus Pelikan ◽  
Meriel J. Bittner ◽  
Thomas Reinthaler ◽  
Martin Könneke ◽  
...  

ABSTRACT Ammonia-oxidizing archaea (AOA) play an important role in the nitrogen cycle and account for a considerable fraction of the prokaryotic plankton in the ocean. Most AOA lack the hydrogen peroxide (H2O2)-detoxifying enzyme catalase, and some AOA have been shown to grow poorly under conditions of exposure to H2O2. However, differences in the degrees of H2O2 sensitivity of different AOA strains, the physiological status of AOA cells exposed to H2O2, and their molecular response to H2O2 remain poorly characterized. Further, AOA might rely on heterotrophic bacteria to detoxify H2O2, and yet the extent and variety of costs and benefits involved in these interactions remain unclear. Here, we used a proteomics approach to compare the protein profiles of three Nitrosopumilus strains grown in the presence and absence of catalase and in coculture with the heterotrophic alphaproteobacterium Oceanicaulis alexandrii. We observed that most proteins detected at a higher relative abundance in H2O2-exposed Nitrosopumilus cells had no known function in oxidative stress defense. Instead, these proteins were putatively involved in the remodeling of the extracellular matrix, which we hypothesize to be a strategy limiting the influx of H2O2 into the cells. Using RNA-stable isotope probing, we confirmed that O. alexandrii cells growing in coculture with the Nitrosopumilus strains assimilated Nitrosopumilus-derived organic carbon, suggesting that AOA could recruit H2O2-detoxifying bacteria through the release of labile organic matter. Our results contribute new insights into the response of AOA to H2O2 and highlight the potential ecological importance of their interactions with heterotrophic free-living bacteria in marine environments. IMPORTANCE Ammonia-oxidizing archaea (AOA) are the most abundant chemolithoautotrophic microorganisms in the oxygenated water column of the global ocean. Although H2O2 appears to be a universal by-product of aerobic metabolism, genes encoding the hydrogen peroxide (H2O2)-detoxifying enzyme catalase are largely absent in genomes of marine AOA. Here, we provide evidence that closely related marine AOA have different degrees of sensitivity to H2O2, which may contribute to niche differentiation between these organisms. Furthermore, our results suggest that marine AOA rely on H2O2 detoxification during periods of high metabolic activity and release organic compounds, thereby potentially attracting heterotrophic prokaryotes that provide this missing function. In summary, this report provides insights into the metabolic interactions between AOA and heterotrophic bacteria in marine environments and suggests that AOA play an important role in the biogeochemical carbon cycle by making organic carbon available for heterotrophic microorganisms.


Genes ◽  
2021 ◽  
Vol 12 (6) ◽  
pp. 855
Author(s):  
Mikołaj Kokociński ◽  
Dariusz Dziga ◽  
Adam Antosiak ◽  
Janne Soininen

Bacterioplankton community composition has become the center of research attention in recent years. Bacteria associated with toxic cyanobacteria blooms have attracted considerable interest. However, little is known about the environmental factors driving the bacteria community, including the impact of invasive cyanobacteria. Therefore, our aim has been to determine the relationships between heterotrophic bacteria and phytoplankton community composition across 24 Polish lakes with different contributions of cyanobacteria including the invasive species Raphidiopsis raciborskii. This analysis revealed that cyanobacteria were present in 16 lakes, while R. raciborskii occurred in 14 lakes. Our results show that bacteria communities differed between lakes dominated by cyanobacteria and lakes with minor contributions of cyanobacteria but did not differ between lakes with R. raciborskii and other lakes. Physical factors, including water and Secchi depth, were the major drivers of bacteria and phytoplankton community composition. However, in lakes dominated by cyanobacteria, bacterial community composition was also influenced by biotic factors such as the amount of R. raciborskii, chlorophyll-a and total phytoplankton biomass. Thus, our study provides novel evidence on the influence of environmental factors and R. raciborskii on lake bacteria communities.


2015 ◽  
Vol 282 (1810) ◽  
pp. 20150371 ◽  
Author(s):  
Xosé Anxelu G. Morán ◽  
Laura Alonso-Sáez ◽  
Enrique Nogueira ◽  
Hugh W. Ducklow ◽  
Natalia González ◽  
...  

Heterotrophic bacteria play a major role in organic matter cycling in the ocean. Although the high abundances and relatively fast growth rates of coastal surface bacterioplankton make them suitable sentinels of global change, past analyses have largely overlooked this functional group. Here, time series analysis of a decade of monthly observations in temperate Atlantic coastal waters revealed strong seasonal patterns in the abundance, size and biomass of the ubiquitous flow-cytometric groups of low (LNA) and high nucleic acid (HNA) content bacteria. Over this relatively short period, we also found that bacterioplankton cells were significantly smaller, a trend that is consistent with the hypothesized temperature-driven decrease in body size. Although decadal cell shrinking was observed for both groups, it was only LNA cells that were strongly coherent, with ecological theories linking temperature, abundance and individual size on both the seasonal and interannual scale. We explain this finding because, relative to their HNA counterparts, marine LNA bacteria are less diverse, dominated by members of the SAR11 clade. Temperature manipulation experiments in 2012 confirmed a direct effect of warming on bacterial size. Concurrent with rising temperatures in spring, significant decadal trends of increasing standing stocks (3% per year) accompanied by decreasing mean cell size (−1% per year) suggest a major shift in community structure, with a larger contribution of LNA bacteria to total biomass. The increasing prevalence of these typically oligotrophic taxa may severely impact marine food webs and carbon fluxes by an overall decrease in the efficiency of the biological pump.


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