scholarly journals Prochlorococcus Cells Rely on Microbial Interactions Rather than on Chlorotic Resting Stages To Survive Long-Term Nutrient Starvation

mBio ◽  
2020 ◽  
Vol 11 (4) ◽  
Author(s):  
Dalit Roth-Rosenberg ◽  
Dikla Aharonovich ◽  
Tal Luzzatto-Knaan ◽  
Angela Vogts ◽  
Luca Zoccarato ◽  
...  
Keyword(s):  
Metabolic Activity ◽  
Heterotrophic Bacteria ◽  
Heterotrophic Bacterium ◽  
N Uptake ◽  
Biogeochemical Cycles ◽  
Nutrient Starvation ◽  
Microbial Interactions ◽  
Resting Cells ◽  
Resting Stages ◽  
Eukaryotic Phytoplankton

ABSTRACT Many microorganisms produce resting cells with very low metabolic activity that allow them to survive phases of prolonged nutrient or energy stress. In cyanobacteria and some eukaryotic phytoplankton, the production of resting stages is accompanied by a loss of photosynthetic pigments, a process termed chlorosis. Here, we show that a chlorosis-like process occurs under multiple stress conditions in axenic laboratory cultures of Prochlorococcus, the dominant phytoplankton linage in large regions of the oligotrophic ocean and a global key player in ocean biogeochemical cycles. In Prochlorococcus strain MIT9313, chlorotic cells show reduced metabolic activity, measured as C and N uptake by Nanoscale secondary ion mass spectrometry (NanoSIMS). However, unlike many other cyanobacteria, chlorotic Prochlorococcus cells are not viable and do not regrow under axenic conditions when transferred to new media. Nevertheless, cocultures with a heterotrophic bacterium, Alteromonas macleodii HOT1A3, allowed Prochlorococcus to survive nutrient starvation for months. We propose that reliance on co-occurring heterotrophic bacteria, rather than the ability to survive extended starvation as resting cells, underlies the ecological success of Prochlorococcus. IMPORTANCE The ability of microorganisms to withstand long periods of nutrient starvation is key to their survival and success under highly fluctuating conditions that are common in nature. Therefore, one would expect this trait to be prevalent among organisms in the nutrient-poor open ocean. Here, we show that this is not the case for Prochlorococcus, a globally abundant and ecologically important marine cyanobacterium. Instead, Prochlorococcus relies on co-occurring heterotrophic bacteria to survive extended phases of nutrient and light starvation. Our results highlight the power of microbial interactions to drive major biogeochemical cycles in the ocean and elsewhere with consequences at the global scale.

scholarly journals Prochlorococcus rely on microbial interactions rather than on chlorotic resting stages to survive long-term nutrient starvation

2019 ◽  
Author(s):  
Dalit Roth-Rosenberg ◽  
Dikla Aharonovich ◽  
Tal Luzzatto-Knaan ◽  
Angela Vogts ◽  
Luca Zoccarato ◽  
...  
Keyword(s):  
Metabolic Activity ◽  
Heterotrophic Bacteria ◽  
Heterotrophic Bacterium ◽  
N Uptake ◽  
Biogeochemical Cycles ◽  
Nutrient Starvation ◽  
Microbial Interactions ◽  
Resting Cells ◽  
Resting Stages ◽  
Eukaryotic Phytoplankton

AbstractMany microorganisms produce resting cells with very low metabolic activity that allow them to survive phases of prolonged nutrient or energy stress. In cyanobacteria and some eukaryotic phytoplankton, the production of resting stages is accompanied by a loss of photosynthetic pigments, a process termed chlorosis. Here, we show that a chlorosis-like process occurs under multiple stress conditions in axenic laboratory cultures of Prochlorococcus, the dominant phytoplankton linage in large regions of the oligotrophic ocean and a global key player in ocean biogeochemical cycles. In Prochlorococcus strain MIT9313, chlorotic cells show reduced metabolic activity, measured as C and N uptake by NanoSIMS. However, unlike many other cyanobacteria, chlorotic Prochlorococcus cells are not viable and do not re-grow under axenic conditions when transferred to new media. Nevertheless, co-cultures with a heterotrophic bacterium, Alteromonas macleodii HOT1A3, allowed Prochlorococcus to survive nutrient starvation for months. We propose that reliance on co-occurring heterotrophic bacteria, rather than the ability to survive extended starvation as resting cells, underlies the ecological success of Prochlorococcus.ImportanceThe ability of microorganisms to withstand long periods of nutrient starvation is key to their survival and success under highly fluctuating conditions as is common in nature. Therefore, one would expect this trait to be prevalent among organisms in the nutrient-poor open ocean. Here, we show that this is not the case for Prochlorococcus, a globally abundant and ecologically impactful marine cyanobacterium. Instead, Prochlorococcus rely on co-occurring heterotrophic bacteria to survive extended phases of nutrient and light starvation. Our results highlight the power of microbial interactions to drive major biogeochemical cycles in the ocean and elsewhere with consequences at the global scale.

Denitrification by a novel halophilic fermentative bacterium

1996 ◽  
Vol 42 (5) ◽  
pp. 507-514 ◽  
Author(s):  
Wung Yang Shieh ◽  
Chia Ming Liu
Keyword(s):  
National Park ◽  
Heterotrophic Bacteria ◽  
Heterotrophic Bacterium ◽  
Halophilic Bacteria ◽  
Anaerobic Growth ◽  
Anaerobic Conditions ◽  
Early Stationary Phase ◽  
Gram Negative ◽  
Fermentative Bacteria ◽  
Curved Rods

A novel halophilic heterotrophic bacterium, designated strain DN34, was isolated from seawater in Nanwan Bay of Renting National Park, Taiwan. It was Gram negative and facultatively anaerobic. Cells in late exponential to early stationary phase of growth were predominantly straight or curved rods, but Y- or V-shaped forms were also observed; straight and curved rods achieved motility by one to several lateral or subpolar flagella. The G+C content of the DNA was 51.7 mol%. Strain DN34 grew optimally at about 30 °C and pH 8.0. Growth depended on the presence of NaCl with optimal concentration at about 3%. Aerobically, strain DN34 grew much better and tolerated NaCl at a greater range of concentration with sufficient Mg2+and Ca2+than under deficient conditions; Mg2+or Ca2+was indispensable for growth under anaerobic conditions. The strain was capable of anaerobic growth by carrying out denitrifying metabolism using nitrate, nitrite, or nitrous oxide as terminal electron acceptors or, alternatively, by fermenting glucose or mannose as substrates. Halophilic heterotrophic bacteria capable of both denitrification and fermentation have not been reported previously.Key words: denitrification, denitrifying bacteria, halophilic bacteria, fermentative bacteria.

scholarly journals Isolation and Characterization of Crude Oil Degrading Bacteria in Association with Microalgae in Saver Pit from Egbaoma Flow Station, Niger Delta, Nigeria

2020 ◽  
Vol 2 (2) ◽  
pp. 12-16
Author(s):  
Obhioze Augustine Akpoka
Keyword(s):  
Crude Oil ◽  
Heterotrophic Bacteria ◽  
Oil Pollution ◽  
Heterotrophic Bacterium ◽  
Bacterial Species ◽  
Carbon Sources ◽  
Sole Source ◽  
Isolation And Characterization ◽  
Degrading Bacteria ◽  
Hydrocarbon Utilizing Bacteria

The capability of indigenous bacteria and microalgae in crude oil effluents to grow in and utilize crude oil as their sole source of carbon and energy provides an environmentally friendly and economical process for dealing with crude oil pollution and its inherent hazards. In view of the toxicity of crude oil spillages to indwellers of the affected ecosystems and the entire affected environment, the isolation of pure bacterial and microalgae cultures from crude effluents is a step in the right direction, particularly for bio-augmentation or bioremediation purposes. The total heterotrophic bacteria count and hydrocarbon utilizing bacteria count, as well as the microalgae count, were determined with the pour plate technique. The physicochemical properties of the effluent samples were also analyzed. Identification of the hydrocarbon utilizing bacteria was performed with phenotypic techniques. The result shows a mean total heterotrophic bacterium count of 5.91 log CFU/ml and a mean microalga count of 4.77 log cells/ml. When crude oil and polycyclic aromatic hydrocarbon (PAH) were used as sole carbon sources, total hydrocarbon utilizing bacteria counts were respectively estimated at 3.89 and 2.89 log CFU/ml. Phenotypic identification of hydrocarbon utilizing bacteria in the crude oil effluents revealed the presence of two main bacterial genera: Streptococcus and Pseudomonas. Data obtained from this study confirmed the biodegradative abilities of indigenous bacterial species, thus, ultimately resulting in the amelioration of the toxicity associated with the crude oil effluents.

Biofilms in Sewer Systems – Characterization of the Bacterial Biocenosis and Its Metabolic Activity

1994 ◽  
Vol 29 (7) ◽  
pp. 385-388 ◽  
Author(s):  
D. Roth ◽  
H. Lemmer
Keyword(s):  
Metabolic Activity ◽  
Heterotrophic Bacteria ◽  
Anaerobic Bacteria ◽  
Population Densities ◽  
Sewer Systems ◽  
Solid Media ◽  
Alanine Aminopeptidase ◽  
High Concentrations ◽  
Metabolic Activities

Biofilms sampled from sewers discharging domestic and trade wastewater, respectively, were characterized by determining the population densities of different groups of heterotrophic bacteria as well as by measuring their metabolic activities. Population densities of heterotrophic saprophytes, of proteolytic, amylolytic, and lipolytic bacteria as well as of ammonifying, nitrate reducing and anaerobic bacteria were determined on solid media and by MPN-tests. Metabolic activity was assessed by measuring enzyme activity of esterase, L-alanine-aminopeptidase, phosphatase, as well as of α- and β-glucosidase. Both biofilms revealed high population densities of bacteria from several metabolic groups as well as high enzyme activities. Their heterotrophic activity is in the range of or even higher than that found in high load activated sludges. The high activity of the bacterial biocenosis proves its resistance against high concentrations of chromium and nickel.

Eco-physiology of autotrophic nitrifying biofilms

2005 ◽  
Vol 52 (7) ◽  
pp. 225-232 ◽  
Author(s):  
S. Okabe ◽  
T. Kindaichi ◽  
Y. Nakamura ◽  
T. Ito
Keyword(s):  
Organic Matter ◽  
Fluorescent In Situ Hybridization ◽  
Direct Evidence ◽  
Heterotrophic Bacteria ◽  
Microbial Interactions ◽  
Nitrifying Bacteria ◽  
Low Molecular Weight ◽  
Sulfur Bacteria ◽  
First Time

Microautoradiography combined with fluorescent in situ hybridization (MAR-FISH), a powerful tool for linking physiology with identification of individual cells, was applied to investigate microbial interactions between nitrifying bacteria and coexisting heterotrophic bacteria in an autotrophic nitrifying biofilm community fed with only ammonia as the sole energy source and bicarbonate as the sole carbon source. First, nitrifying bacteria were radiolabeled by culturing the biofilm samples with [14C]bicarbonate for 6 h, and then the transfer of radioactivity from nitrifying bacteria to heterotrophic bacteria was monitored by using MAR-FISH. MAR-FISH revealed that the heterotrophic bacterial community was composed of bacteria that were phylogenetically and metabolically diverse. We could obtain direct evidence that organic matter derived from nitrifiers was subsequently utilized by mainly filamentous bacteria belonging to the Chloroflexi (green non-sulfur bacteria) group or CFB group in the biofilm, which was clearly visualized by MAR-FISH at single cell resolution for the first time. On the other hand, the members of the α- and γ-Proteobacteria were specialized to utilize low-molecular-weight organic matter. This community represents functionally integrated units that assure maximum access to and utilization of metabolites of nitrifiers.

Beneficial cyanosphere heterotrophs accelerate establishment of cyanobacterial biocrust

2021 ◽  
Author(s):  
Corey Nelson ◽  
Ferran Garcia-Pichel
Keyword(s):  
Heterotrophic Bacteria ◽  
Microbial Interactions ◽  
Disturbed Areas ◽  
Essential Services ◽  
The Family ◽  
Dryland Ecosystems ◽  
Native Soils ◽  
Soil Substrates ◽  
Potential Use

Biological soil crusts (biocrusts) are communities of microbes that inhabit the surface of arid soils and provide essential services to dryland ecosystems. While resistant to extreme environmental conditions, biocrusts are susceptible to anthropogenic disturbances that can deprive ecosystems of these valuable services for decades. Until recently, culture-based efforts to produce inoculum for cyanobacterial biocrust restoration in the Southwestern US focused on producing and inoculating the most abundant primary producers and biocrust pioneers, Microcoleus vaginatus and members of the family Coleofasciculaceae (aka “ Microcoleus streenstrupii complex”). The discovery that a unique microbial community characterized by diazotrophs is intimately associated with M. vaginatus , known as the “cyanosphere”, suggests a symbiotic division of labor in which nutrients are traded between phototrophs and heterotrophs. To probe the potential use of such cyanosphere members in the restoration of biocrusts, we performed co-inoculations of soil substrates with cyanosphere constituents. This resulted in more rapid cyanobacterial growth over inoculations with the cyanobacterium alone. Additionally, we found that the mere addition of beneficial heterotrophs enhanced the formation of a cohesive biocrust without the need of additional phototrophic biomass within native soils that contain trace amounts of biocrust cyanobacteria. Our findings support the hitherto unknown role of beneficial heterotrophic bacteria in the establishment and growth of biocrusts and allow us to make recommendations concerning biocrust restoration efforts based on the presence of remnant biocrust communities in disturbed areas. Future biocrust restoration efforts should consider cyanobacteria and their beneficial heterotrophic community as inoculants. Importance The advancement of biocrust restoration methodologies for cyanobacterial biocrusts has been largely achieved through trial and error. Successes and failures could not always be traced back to particular factors. The investigation and application of foundational microbial interactions existing within biocrust communities is a crucial step toward informed and repeatable biocrust restoration methodologies.

scholarly journals An Amoebal Grazer of Cyanobacteria Requires Cobalamin Produced by Heterotrophic Bacteria

2017 ◽  
Vol 83 (10) ◽  
Author(s):  
Amy T. Ma ◽  
Joris Beld ◽  
Bianca Brahamsha
Keyword(s):  
Food Webs ◽  
Food Source ◽  
Heterotrophic Bacteria ◽  
Heterotrophic Bacterium ◽  
Content Type ◽  
Predator Prey ◽  
Deletion Mutations ◽  
Microbial Food Webs ◽  
Rich Media ◽  
Insight Into

ABSTRACT Amoebae are unicellular eukaryotes that consume microbial prey through phagocytosis, playing a role in shaping microbial food webs. Many amoebal species can be cultivated axenically in rich media or monoxenically with a single bacterial prey species. Here, we characterize heterolobosean amoeba LPG3, a recent natural isolate, which is unable to grow on unicellular cyanobacteria, its primary food source, in the absence of a heterotrophic bacterium, a Pseudomonas species coisolate. To investigate the molecular basis of this requirement for heterotrophic bacteria, we performed a screen using the defined nonredundant transposon library of Vibrio cholerae, which implicated genes in corrinoid uptake and biosynthesis. Furthermore, cobalamin synthase deletion mutations in V. cholerae and the Pseudomonas species coisolate do not support the growth of amoeba LPG3 on cyanobacteria. While cyanobacteria are robust producers of a corrinoid variant called pseudocobalamin, this variant does not support the growth of amoeba LPG3. Instead, we show that it requires cobalamin that is produced by the Pseudomonas species coisolate. The diversity of eukaryotes utilizing corrinoids is poorly understood, and this amoebal corrinoid auxotroph serves as a model for examining predator-prey interactions and micronutrient transfer in bacterivores underpinning microbial food webs. IMPORTANCE Cyanobacteria are important primary producers in aquatic environments, where they are grazed upon by a variety of phagotrophic protists and, hence, have an impact on nutrient flux at the base of microbial food webs. Here, we characterize amoebal isolate LPG3, which consumes cyanobacteria as its primary food source but also requires heterotrophic bacteria as a source of corrinoid vitamins. Amoeba LPG3 specifically requires the corrinoid variant produced by heterotrophic bacteria and cannot grow on cyanobacteria alone, as they produce a different corrinoid variant. This same corrinoid specificity is also exhibited by other eukaryotes, including humans and algae. This amoebal model system allows us to dissect predator-prey interactions to uncover factors that may shape microbial food webs while also providing insight into corrinoid specificity in eukaryotes.

scholarly journals Biofilm Interactions between Distinct Bacterial Genera Isolated from Drinking Water

2007 ◽  
Vol 73 (19) ◽  
pp. 6192-6200 ◽  
Author(s):  
Lúcia Chaves Simões ◽  
Manuel Simões ◽  
Maria João Vieira
Keyword(s):  
Growth Rate ◽  
Drinking Water ◽  
Metabolic Activity ◽  
Biofilm Formation ◽  
Burkholderia Cepacia ◽  
Water Environment ◽  
16S Rrna Gene Sequencing ◽  
Microbial Interactions ◽  
Rrna Gene ◽  
Bacterial Growth Rate

ABSTRACT In the environment, multiple microorganisms coexist as communities, competing for resources and often associated as biofilms. In this study, single- and dual-species biofilm formation by, and specific activities of, six heterotrophic intergeneric bacteria were determined using 96-well polystyrene plates over a 72-h period. These bacteria were isolated from drinking water and identified by partial 16S rRNA gene sequencing. A series of planktonic studies was also performed, assessing the bacterial growth rate, motility, and production of quorum-sensing inhibitors (QSI). This constituted an attempt to identify key attributes allowing bacteria to effectively interact and coexist in a drinking-water environment. We observed that in both pure and dual cultures, all of the isolates formed stable biofilms within 72 h, with specific metabolic activity decreasing, in most cases, with an increase in biofilm mass. The largest single- and dual-biofilm amounts were found for Methylobacterium sp. and the combination of Methylobacterium sp. and Mycobacterium mucogenicum, respectively. Evidences of microbial interactions in dual-biofilm formation, associated with appreciable biomass variation in comparison with single biofilms, were found for the following cases: synergy/cooperation between Sphingomonas capsulata and Burkholderia cepacia, S. capsulata and Staphylococcus sp., and B. cepacia and Acinetobacter calcoaceticus and antagonism between S. capsulata and M. mucogenicum, S. capsulata and A. calcoaceticus, and M. mucogenicum and Staphylococcus sp. A neutral interaction was found for Methylobacterium sp.-M. mucogenicum, S. capsulata-Staphylococcus sp., M. mucogenicum-A. calcoaceticus, and Methylobacterium sp.-A. calcoaceticus biofilms, since the resultant dual biofilms had a mass and specific metabolic activity similar to the average for each single biofilm. B. cepacia had the highest growth rate and motility and produced QSI. Other bacteria producing QSI were Methylobacterium sp., S. capsulata, and Staphylococcus sp. However, only for S. capsulata-M. mucogenicum, S. capsulata-A. calcoaceticus, and M. mucogenicum-Staphylococcus sp., dual-biofilm formation seems to be regulated by the QSI produced by S. capsulata and Staphylococcus sp. and by the increased growth rate of S. capsulata. The parameters assessed by planktonic studies did not allow prediction and generalization of the exact mechanism regulating dual-species biofilm formation between the drinking-water bacteria.

scholarly journals Broad phylogenetic and functional diversity among mixotrophic consumers of Prochlorococcus

2021 ◽  
Author(s):  
Qian Li ◽  
Kyle F Edwards ◽  
Christopher R Schvarcz ◽  
Grieg F Steward
Keyword(s):  
Euphotic Zone ◽  
Biogeochemical Cycles ◽  
Body Volume ◽  
North Pacific Subtropical Gyre ◽  
The North ◽  
Quantitative Studies ◽  
Eukaryotic Phytoplankton ◽  
Station Aloha ◽  
Functionally Diverse ◽  
The North Pacific

Small eukaryotic phytoplankton are major contributors to global primary production and marine biogeochemical cycles. Many taxa are thought to be mixotrophic, but quantitative studies of phagotrophy exist for very few. In addition, little is known about consumers of Prochlorococcus, the abundant cyanobacterium at the base of oligotrophic ocean food webs. Here we describe thirty–nine new phytoplankton isolates from the North Pacific Subtropical Gyre (Station ALOHA), all flagellates ~2–5 μm diameter, and we quantify their ability to graze Prochlorococcus. The mixotrophs are from diverse classes (dictyochophytes, haptophytes, chrysophytes, bolidophytes, a dinoflagellate, and a chlorarachniophyte), many from previously uncultured clades. Grazing ability varied substantially, with specific clearance rate (volume cleared per body volume) varying over ten–fold across isolates and six–fold across genera. Slower grazers tend to create more biovolume per prey biovolume consumed. Using qPCR we found that the haptophyte Chrysochromulina was most abundant among the isolated mixotrophs at Station ALOHA, with 76–250 cells mL-1 across depths in the upper euphotic zone. Our results show that within a single ecosystem the phototrophs that ingest bacteria come from many branches of the eukaryotic tree, and are functionally diverse, indicating a broad range of strategies along the spectrum from phototrophy to phagotrophy.

scholarly journals Heterotroph Interactions AlterProchlorococcusTranscriptome Dynamics during Extended Periods of Darkness

mSystems ◽  
2018 ◽  
Vol 3 (3) ◽  
Author(s):  
Steven J. Biller ◽  
Allison Coe ◽  
Sara E. Roggensack ◽  
Sallie W. Chisholm
Keyword(s):  
Stress Responses ◽  
Heterotrophic Bacterium ◽  
Biotic Interactions ◽  
Euphotic Zone ◽  
Microbial Interactions ◽  
Ecological Communities ◽  
Community Interactions ◽  
Content Type ◽  
Photosynthetic Organism ◽  
Pure Cultures

ABSTRACTMicrobes evolve within complex ecological communities where biotic interactions impact both individual cells and the environment as a whole. Here we examine how cellular regulation in the marine cyanobacteriumProchlorococcusis influenced by a heterotrophic bacterium,Alteromonas macleodii, under different light conditions. We monitored the transcriptome ofProchlorococcus, grown either alone or in coculture, across a diel light:dark cycle and under the stress of extended darkness—a condition that cells would experience when mixed below the ocean’s euphotic zone. MoreProchlorococcustranscripts exhibited 24-h periodic oscillations in coculture than in pure culture, both over the normal diel cycle and after the shift to extended darkness. This demonstrates that biotic interactions, and not just light, can affect timing mechanisms inProchlorococcus, which lacks a self-sustaining circadian oscillator. The transcriptomes of replicate pure cultures ofProchlorococcuslost their synchrony within 5 h of extended darkness and reflected changes in stress responses and metabolic functions consistent with growth cessation. In contrast, when grown withAlteromonas, replicateProchlorococcustranscriptomes tracked each other for at least 13 h in the dark and showed signs of continued biosynthetic and metabolic activity. The transcriptome patterns suggest that the heterotroph may be providing energy or essential biosynthetic substrates toProchlorococcusin the form of organic compounds, sustaining this autotroph when it is deprived of solar energy. Our findings reveal conditions where mixotrophic metabolism may benefit marine cyanobacteria and highlight new impacts of community interactions on basicProchlorococcuscellular processes.IMPORTANCEProchlorococcusis the most abundant photosynthetic organism on the planet. These cells play a central role in the physiology of surrounding heterotrophs by supplying them with fixed organic carbon. It is becoming increasingly clear, however, that interactions with heterotrophs can affect autotrophs as well. Here we show that such interactions have a marked impact on the response ofProchlorococcusto the stress of extended periods of darkness, as reflected in transcriptional dynamics. These data suggest that diel transcriptional rhythms withinProchlorococcus, which are generally considered to be strictly under the control of light quantity, quality, and timing, can also be influenced by biotic interactions. Together, these findings provide new insights into the importance of microbial interactions onProchlorococcusphysiology and reveal conditions where heterotroph-derived compounds may support autotrophs—contrary to the canonical autotroph-to-heterotroph trophic paradigm.

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