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Ferro, L., Colombo, M., Posadas, E., Funk, C. & Muñoz, R. (2019). Elucidating the symbiotic interactions between a locally isolated microalga Chlorella vulgaris and its co-occurring bacterium Rhizobium sp. in synthetic municipal wastewater. Journal of Applied Phycology, 31(4), 2299-2310
Open this publication in new window or tab >>Elucidating the symbiotic interactions between a locally isolated microalga Chlorella vulgaris and its co-occurring bacterium Rhizobium sp. in synthetic municipal wastewater
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2019 (English)In: Journal of Applied Phycology, ISSN 0921-8971, E-ISSN 1573-5176, Vol. 31, no 4, p. 2299-2310Article in journal (Refereed) Published
Abstract [en]

Co-cultivation of microalgae and bacteria during municipal wastewater treatment can boost carbon and nutrient recovery as a result of their synergistic interactions. The symbiotic relationships between the locally isolated microalga Chlorella vulgaris and the bacterium Rhizobium sp., co-isolated from municipal wastewater, were investigated batchwise under photoautotrophic, heterotrophic, and mixotrophic conditions in a synthetic municipal wastewater medium. During photoautotrophic growth in BG11 medium, photosynthetic algal oxygenation and organic carbon production supported bacterial activity but no significant beneficial effects on microalgal growth were observed. In synthetic wastewater, a twofold higher biomass concentration was achieved in the axenic algal culture compared with the co-culture under heterotrophic conditions, suggesting a competition for nutrients. A comparable carbon removal was observed in all cultures (83–79% TOC), but a faster nitrogen consumption (59% TN) and complete phosphate assimilation (100% TP) was only achieved in the co-culture. A positive synergistic relationship was found under mixotrophic conditions, clearly supported by an in situ O2/CO2 exchange between the microorganisms. This mutualism led to a threefold higher biomass production with a 13-fold higher fatty acid content compared with the axenic algal culture, as well as a superior wastewater treatment performance (+ 58% TOC, + 41% TN and + 44% TP). The co-cultivation of C. vulgaris and Rhizobium is therefore suggested as a potential microbial consortium for a cost-efficient biomass generation during municipal wastewater reclamation, especially under mixotrophic conditions.

Place, publisher, year, edition, pages
Springer, 2019
Keywords
Chlorella vulgaris, Rhizobium, Symbiosis, Mixotrophy, Heterotrophy, Wastewater treatment
National Category
Microbiology Oceanography, Hydrology and Water Resources
Identifiers
urn:nbn:se:umu:diva-156463 (URN)10.1007/s10811-019-1741-1 (DOI)000479057200012 ()
Funder
Swedish Energy Agency, 476 38239-1Swedish Research Council Formas, 942-2015-92
Available from: 2019-02-15 Created: 2019-02-15 Last updated: 2019-08-30Bibliographically approved
Lage, S., Kudahettige, N. P., Ferro, L., Matsakas, L., Funk, C., Rova, U. & Gentili, F. G. (2019). Microalgae Cultivation for the Biotransformation of Birch Wood Hydrolysate and Dairy Effluent. Catalysts, 9(2), Article ID 150.
Open this publication in new window or tab >>Microalgae Cultivation for the Biotransformation of Birch Wood Hydrolysate and Dairy Effluent
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2019 (English)In: Catalysts, E-ISSN 2073-4344, Vol. 9, no 2, article id 150Article in journal (Refereed) Published
Abstract [en]

In order to investigate environmentally sustainable sources of organic carbon and nutrients, four Nordic green microalgal strains, Chlorella sorokiniana, Chlorella saccharophila, Chlorella vulgaris, and Coelastrella sp., were grown on a wood (Silver birch, Betula pendula) hydrolysate and dairy effluent mixture. The biomass and lipid production were analysed under mixotrophic, as well as two-stage mixotrophic/heterotrophic regimes. Of all of the species, Coelastrella sp. produced the most total lipids per dry weight (~40%) in the mixture of birch hydrolysate and dairy effluent without requiring nutrient (nitrogen, phosphorus, and potassium—NPK) supplementation. Overall, in the absence of NPK, the two-stage mixotrophic/heterotrophic cultivation enhanced the lipid concentration, but reduced the amount of biomass. Culturing microalgae in integrated waste streams under mixotrophic growth regimes is a promising approach for sustainable biofuel production, especially in regions with large seasonal variation in daylight, like northern Sweden. To the best of our knowledge, this is the first report of using a mixture of wood hydrolysate and dairy effluent for the growth and lipid production of microalgae in the literature.

Place, publisher, year, edition, pages
MDPI, 2019
Keywords
mixotrophic, heterotrophic, lipids, fatty acid methyl esters, dairy wastewater, birch hydrolysate, green algae, Coelastrella, Chlorella
National Category
Bioenergy
Identifiers
urn:nbn:se:umu:diva-157784 (URN)10.3390/catal9020150 (DOI)000460702200044 ()2-s2.0-85062564536 (Scopus ID)
Projects
Bio4Energy
Available from: 2019-04-03 Created: 2019-04-03 Last updated: 2019-09-06Bibliographically approved
Ferro, L., Miranda, F., Gentili, F. & Funk, C. (2019). Photosynthesis at high latitudes: adaptation of photosynthetic microorganisms to Nordic climates. In: Biotechnological Applications of Extremophilic Microorganisms: Life in Extreme Environments. Walter de Gruyter
Open this publication in new window or tab >>Photosynthesis at high latitudes: adaptation of photosynthetic microorganisms to Nordic climates
2019 (English)In: Biotechnological Applications of Extremophilic Microorganisms: Life in Extreme Environments, Walter de Gruyter, 2019Chapter in book (Other academic)
Place, publisher, year, edition, pages
Walter de Gruyter, 2019
National Category
Microbiology
Identifiers
urn:nbn:se:umu:diva-156469 (URN)978-3-11-042773-8 (ISBN)
Available from: 2019-02-15 Created: 2019-02-15 Last updated: 2019-02-19
Martínez, J. M., Gojkovic, Z., Ferro, L., Maza, M., Alvarez, I., Raso, J. & Funk, C. (2019). Use of pulsed electric field permeabilization to extract astaxanthin from the Nordic microalga Haematococcus pluvialis. Bioresource Technology, 289, Article ID 121694.
Open this publication in new window or tab >>Use of pulsed electric field permeabilization to extract astaxanthin from the Nordic microalga Haematococcus pluvialis
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2019 (English)In: Bioresource Technology, ISSN 0960-8524, E-ISSN 1873-2976, Vol. 289, article id 121694Article in journal (Refereed) Published
Abstract [en]

The Nordic microalgal strain Haematococcus pluvialis was exposed to various stress conditions to induce astaxanthin accumulation. Highest carotenoid content (19.1 mg·g−1dw) was achieved in nitrogen-free culture medium at a high light intensity. The efficiency of Pulsed Electric Field (PEF) pre-treatment of stressed fresh biomass of H. pluvialis followed by incubation in the growth medium was compared to classical disruption methods (bead-beating, freezing-thawing, thermal treatment or ultrasound) for the subsequent extraction of astaxanthin in ethanol. N-starved cells treated with PEF followed by aqueous incubation for 6 h resulted in extraction of 96% (18.3 mgcar·gdw−1) of the total carotenoid content compared to 80% (15.3 mgcar·gdw−1) using other physical methods. The proportion of free forms of astaxanthin was higher in PEF-treated samples compared to mechanical disruption, suggesting PEF triggering an esterase activity. PEF pre-treatment of the cells followed by incubation in growth medium improved astaxanthin extraction in the eco-friendly solvent ethanol.

Place, publisher, year, edition, pages
Elsevier, 2019
Keywords
Astaxanthin, Pulsed electric field (PEF), Microalgae, Incubation, Extraction
National Category
Food Science
Identifiers
urn:nbn:se:umu:diva-161873 (URN)10.1016/j.biortech.2019.121694 (DOI)000475746800135 ()31254897 (PubMedID)2-s2.0-85067837146 (Scopus ID)
Available from: 2019-08-08 Created: 2019-08-08 Last updated: 2019-08-08Bibliographically approved
Ferro, L. (2019). Wastewater treatment and biomass generation by Nordic microalgae: growth in subarctic climate and microbial interactions. (Doctoral dissertation). Umeå: Umeå University
Open this publication in new window or tab >>Wastewater treatment and biomass generation by Nordic microalgae: growth in subarctic climate and microbial interactions
2019 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Nordic native microalgal strains were isolated, genetically classified and tested for their ability to grow in municipal wastewater. Eight of the isolated strains could efficiently remove nitrogen and phosphate in less than two weeks. Two of these strains, Coelastrella sp. and Chlorella vulgaris, were found to have high biomass concentration and total lipid content; also two Desmodesmus sp. strains showed desirable traits for biofuel-feedstock, due to their fast growth rates and high oil content.

The adaptation to subarctic climate was comparatively evaluated in three Nordic strains (C. vulgaris, Scenedesmus sp. and Desmodesmus sp.) and a collection strain (S. obliquus). Their growth performance, biomass composition and nutrients removal was investigated at standard (25°C) or low temperature (5°C), under continuous light at short photoperiod (3 h light, 25°C) or moderate winter conditions (6 h light, 15°C). Only the Nordic strains could grow and produce biomass at low temperature, and efficiently removed nitrogen and phosphate during both cold- and dark-stress. Phenotypic plasticity was observed in Scenedesmus and Desmodesmus under different growth conditions, adaptation to low temperature increased their carbohydrate content. Short photoperiod strongly reduced growth rates, biomass and storage compounds in all strains and induced flocculation in C. vulgaris, which, however, performed best under moderate winter conditions.

The symbiotic relationships between the Nordic microalga C. vulgaris and the naturally co-occurring bacterium Rhizobium sp. were investigated batchwise under photoautotrophic, heterotrophic and mixotrophic conditions, comparing the co-culture to the axenic cultures. The photoautotrophic algal growth in BG11 medium mainly supported Rhizobium activity in the co-culture, with no significant effects on C. vulgaris. In synthetic wastewater, a synergistic interaction only occurred under mixotrophic conditions, supported by CO2/O2 exchange and a lower pH in the culture, resulting in higher biomass and fatty acids content and more efficient wastewater treatment in the co-culture. Under heterotrophic conditions, the lower biomass production in the co-culture suggested a competition for nutrients, although nutrients removal remained efficient.

A pilot-scale high rate algal pond (HRAP) located in Northern Sweden was inoculated with the collection strain Scenedesmus dimorphus UTEX 417 and operated from spring to autumn. Using metabarcoding of 18S and 16S rRNA genes, the microbial diversity of eukaryotic and prokaryotic communities was revealed. S. dimorphus was initially stable in the culture, but other microalgal species later colonized the system, mainly due to parasitic infections and predation by zooplankton in summer. The main competitor algal species were Desmodesmus, Pseudocharaciopsis, Chlorella, Characium and Oocystis. Proteobacteria, Firmicutes, Bacteroidetes and Actinobacteria were the most abundant bacterial phyla in the HRAP. The structure of the microbial communities followed a seasonal variation and partially correlated to environmental factors such as light, temperature and nutrients concentrations.

Overall, these results contribute with new knowledge on the establishment and optimization of microalgal-based wastewater treatment systems coupled with biomass generation in Nordic areas. The use of native microalgal species is proposed as a potential strategy to overcome the limitations posed to algal cultivation in subarctic regions.

Place, publisher, year, edition, pages
Umeå: Umeå University, 2019. p. 75
Keywords
Microalgae, Wastewater, Nitrogen, Phosphate, Biomass, Lipids, Subarctic Climate, Light, Temperature, Bacteria, Photoautotrophy, Heterotrophy, Mixotrophy, HRAP, Metabarcoding, Microbial Communities, Alpha-diversity, Environmental Factors
National Category
Microbiology Other Biological Topics Biochemistry and Molecular Biology Chemical Sciences
Research subject
Biochemistry; Microbiology
Identifiers
urn:nbn:se:umu:diva-156470 (URN)978-91-7855-014-2 (ISBN)
Public defence
2019-03-15, Carl Kempe salen (KB.E3.03), KBC-huset, Umeå, 10:00 (English)
Opponent
Supervisors
Available from: 2019-02-22 Created: 2019-02-15 Last updated: 2019-02-21Bibliographically approved
Ferro, L., Gentili, F. G. & Funk, C. (2018). Isolation and characterization of microalgal strains for biomass production and wastewater reclamation in Northern Sweden. Algal Research, 32, 44-53
Open this publication in new window or tab >>Isolation and characterization of microalgal strains for biomass production and wastewater reclamation in Northern Sweden
2018 (English)In: Algal Research, ISSN 2211-9264, Vol. 32, p. 44-53Article in journal (Refereed) Published
Abstract [en]

Microalgal strains adapted to the harsh Nordic climate were isolated from Swedish fresh- and wastewater sources and tested for their ability to grow in municipal wastewater. The 62 strains able to grow in municipal wastewater belonged to 12 different genera, of those Desmodesmus, Scenedesmus and Chlorella were most representative. Eight axenic strains were further characterized, all of which could efficiently remove nitrogen (>90%) and phosphate (>99%) from the wastewater in less than two weeks. The microalga Coelastrella sp. had the highest performance in terms of both biomass concentration and total lipid content (1.46 g/L, 30.8%) after 13 days of cultivation. This is the first report of a Coelastrella strain isolated in Sweden. Even Chlorella vulgaris performed very well with a biomass concentration and total lipid content of 1.15 g/L and 34.2%, respectively. Finally, two Desmodesmus sp. strains showed desirable traits for biofuel-feedstock, due to their fast growth rates (1.18 and 1.08 d−1) together with high oil content (29.8% and 36.7% of DW).

Place, publisher, year, edition, pages
Elsevier, 2018
Keywords
Microalgae, Northern Sweden, Municipal wastewater, Biomass production, Nitrogen, Phosphate
National Category
Other Chemistry Topics
Identifiers
urn:nbn:se:umu:diva-145999 (URN)10.1016/j.algal.2018.03.006 (DOI)000432649800005 ()
Projects
Bio4Energy
Available from: 2018-03-26 Created: 2018-03-26 Last updated: 2019-09-06Bibliographically approved
Ferro, L., Gorzsás, A., Gentili, F. G. & Funk, C. (2018). Subarctic microalgal strains treat wastewater and produce biomass at low temperature and short photoperiod. Algal Research, 35, 160-167
Open this publication in new window or tab >>Subarctic microalgal strains treat wastewater and produce biomass at low temperature and short photoperiod
2018 (English)In: Algal Research, ISSN 2211-9264, Vol. 35, p. 160-167Article in journal (Refereed) Published
Abstract [en]

In Northern countries, microalgal-based processes are challenging due to low light and temperature conditions during a significant part of the year. Three natural strains from Northern Sweden (Chlorella vulgaris, Scenedesmus sp., Desmodesmus sp.) and a collection strain (Scenedesmus obliquus UTEX 417) were cultured in municipal wastewater, comparing their performances, biomass composition and nutrients removal under continuous light at standard (25 °C) and low temperature (5 °C), short photoperiod (3 h light, 25 °C), or moderate winter conditions (6 h light, 15 °C). Only the natural strains grew at low temperature, highly consuming total nitrogen and phosphate (>80% and >70%, respectively) even during cold- and dark-stress. At reduced growth rates, C. vulgaris and Scenedesmus sp. produced similar amounts of biomass (>1 g/l) as in standard conditions. Scenedesmus sp. and Desmodesmus sp. showed phenotypic plasticity and increased carbohydrate content. Short photoperiod strongly reduced growth rates, biomass and storage compounds and induced flocculation in C. vulgaris.

Place, publisher, year, edition, pages
Elsevier, 2018
Keywords
Subarctic climate, Microalgae, Wastewater treatment, Temperature, Photoperiod
National Category
Microbiology
Identifiers
urn:nbn:se:umu:diva-153114 (URN)10.1016/j.algal.2018.08.031 (DOI)000447187700016 ()2-s2.0-85052483715 (Scopus ID)
Projects
Bio4Energy
Available from: 2018-11-12 Created: 2018-11-12 Last updated: 2019-09-06Bibliographically approved
Ferro, L., Hu, Y., Gentili, F., Andersson, A. & Funk, C. Microbial population dynamics in a microalgae-based municipal wastewater treatment photobioreactor located in Northern Sweden.
Open this publication in new window or tab >>Microbial population dynamics in a microalgae-based municipal wastewater treatment photobioreactor located in Northern Sweden
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

A pilot-scale high-rate algal pond (HRAP) located in Northern Sweden was inoculated with the collection strain S. dimorphus UTEX 417 in spring and operated until autumn. The microbial diversity of eukaryotic and prokaryotic communities and their seasonal dynamics over time were revealed by high-throughput metabarcoding of 18S and 16S rRNA genes and correlated with various environmental factors. S. dimorphus was initially stable in the culture, but other microalgae appeared later and co-dominate the system as a consequence of predation by zooplankton. Desmodesmus, Pseudocharaciopsis, Chlorella, Characium and Oocystis were the main competing algal species. Proteobacteria, Firmicutes, Bacteroidetes and Actinobacteria were the most abundant bacterial phyla in the HRAP. The bacterial and zooplanktonic communities changed with seasonal variation, correlation not only with changes in light and temperature, but also with abiotic factors (pH and nutrients) were observed.

National Category
Microbiology
Identifiers
urn:nbn:se:umu:diva-156465 (URN)
Funder
Swedish Energy Agency, 38239-1Swedish Research Council Formas, 942-2015-92
Available from: 2019-02-15 Created: 2019-02-15 Last updated: 2019-02-19
Organisations
Identifiers
ORCID iD: ORCID iD iconorcid.org/0000-0002-9481-8537

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