Importance of Species Sorting and Immigration on the Bacterial Assembly of Different-Sized Aggregates in a Full-Scale Aerobic Granular Sludge Plant

Ali, Muhammad; Wang, Zhongwei; Salam, Khaled W.; Hari, Ananda Rao; Pronk, Mario; Loosdrecht, Mark C.M. van; Saikaly, Pascal E.

doi:10.1021/acs.est.8b07303

Cited by 104 publications

(92 citation statements)

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“…Biofilms can establish emerging features not always possible outside the biofilm environment, such as nutrient gradients across trophic groups and aerobic or anaerobic microniches ( 2 ). Classical models of formation and growth of attached biofilms are widely accepted ( 1 , 3 ), but biofilm development and community assembly by complex microbiomes is still of increasing interest ( 4 – 8 ). A challenge for such studies is in identifying highly replicated, complex, and diverse communities that experience identical environmental conditions, especially at scales relevant to cells ( 5 ).…”

Section: Introductionmentioning

confidence: 99%

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confidence: 99%

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Size Shapes the Active Microbiome of Methanogenic Granules, Corroborating a Biofilm Life Cycle

et al. 2020

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Methanogenic archaea are key players in cycling organic matter in nature but also in engineered waste treatment systems, where they generate methane, which can be used as a renewable energy source. In such systems in the built environment, complex methanogenic consortia are known to aggregate into highly organized, spherical granular biofilms comprising the interdependent microbial trophic groups mediating the successive stages of the anaerobic digestion (AD) process. This study separated methanogenic granules into a range of discrete size fractions, hypothesizing different biofilm growth stages, and separately supplied each with specific substrates to stimulate the activity of key AD trophic groups, including syntrophic acid oxidizers and methanogens. Rates of specific methanogenic activity were measured, and amplicon sequencing of 16S rRNA gene transcripts was used to resolve phylotranscriptomes across the series of size fractions. Increased rates of methane production were observed in each of the size fractions when hydrogen was supplied as the substrate compared with those of volatile fatty acids (acetate, propionate, and butyrate). This was connected to a shift toward hydrogenotrophic methanogenesis dominated by Methanobacterium and Methanolinea. Interestingly, the specific active microbiomes measured in this way indicated that size was significantly more important than substrate in driving the structure of the active community in granules. Multivariate integration studywise discriminant analysis identified 56 genera shaping changes in the active community across both substrate and size. Half of those were found to be upregulated in the medium-sized granules, which were also the most active and potentially of the most important size, or life stage, for precision management of AD systems. IMPORTANCE Biological wastewater conversion processes collectively constitute one of the single biggest worldwide applications of microbial communities. There is an obvious requirement, therefore, to study the microbial systems central to the success of such technologies. Methanogenic granules, in particular, are architecturally fascinating biofilms that facilitate highly organized cooperation within the metabolic network of the anaerobic digestion (AD) process and, thus, are especially intriguing model systems for microbial ecology. This study, in a way not previously reported, provoked syntrophic and methanogenic activity and the structure of the microbial community, using specific substrates targeting the key trophic groups in AD. Unexpectedly, granule size more strongly than substrate shaped the active portion of the microbial community. Importantly, the findings suggest the size, or age, of granules inherently shapes the active microbiome linked to a life cycle. This provides exciting insights into the function of, and the potential for additional modeling of biofilm development in, methanogenic granules.

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Section: Introductionmentioning

confidence: 99%

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confidence: 99%

Size Shapes the Active Microbiome of Methanogenic Granules, Corroborating a Biofilm Life Cycle

et al. 2020

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“…Island biogeography theory is one of the most influential paradigms in ecology, which is central to several disciplines (e.g., conservation ecology and metapopulation theory) and continues to provide insights into research of island-like systems [41][42][43][44]. For example, Ali, Wang, Salam, Hari, Pronk, Van Loosdrecht, Saikaly [44] observed that the species sorting was significantly higher in flocs and small granules than large granules in aerobic granular sludge system, while putative functional populations were enriched with an increase in microbial aggregates size. Here, we adopted the theory of island biogeography as a conceptual framework for understanding the microbial ecology of microbes within a granule-based PN/A bioreactor.…”

Section: Granular Aggregate As a Microscopic Model System For Island mentioning

confidence: 99%

“…Therefore, we hypothesized granules with different sizes represent microscopic islands with different island areas, thus affecting microbial diversity and functional diversity [17,18].…”

Section: Introductionmentioning

confidence: 99%

Island biogeography on a micro-scale: Larger anammox granules not only harbor higher species diversity but also support more functional diversity

Hui

Liu

et al. 2020

Preprint

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Background: According to the theory of island biogeography, there is a strong relationship between the species diversity and the isolated area. However, it is unclear whether the ecological distribution of microorganisms follows this island biogeography pattern at micro-scale. Here, we use microbial granules harvested from a partial nitritation and anammox (PN/A) system as a model to test if the microbial and functional diversity follow the island biogeography. We collected and divided these granules into five discrete size-fractions (<0.2, 0.2–0.5, 0.5–0.8, 0.8–1.0 and >1.0 mm).Results: By comparing the composition and functional attribute of five pools of the size-fractionated granules by 16S rRNA gene amplicon, metagenomic and metatranscriptomic sequencing, larger granules were shown not only to harbor higher microbial diversity, but also to support more diverse functions than smaller granules. De novo co-assembly and binning of metagenomic reads yielded 22 near-complete genomes of dominant microorganisms, which allowed us to infer an ecological model of the microbial ecosystem in anammox-based granules. This genome-based ecological model indicates that nitrifying organisms in smaller granules feed nitrite to anammox bacteria in larger granules.Conclusion: Our findings substantiate that microbial communities in PN/A granules follow a species-volume relationship, suggesting the generality of the theory of island biogeography on microscopic scale.

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“…Intense interest now surrounds the study of granular biofilms as playgrounds to investigate fundamental concepts in microbial ecology (19). Recent studies (20, 21) have used granules – albeit aerobic, and not anaerobic, granules – to study the roles of phenomena, such as immigration and species sorting, driving microbial community assembly.…”

Section: Introductionmentioning

confidence: 99%

De NovoGrowth of Methanogenic Granules Indicates a Biofilm Life-Cycle with Complex Ecology

Trego

Galvin

Sweeney

et al. 2019

Preprint

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395 words (249 in 'Abstract' + 146 in 'Importance') 8 Text: 3,980 words (excl. references, table footnotes, figure legends) 9Abstract. Methanogenic sludge granules are densely packed, small (diameter, 1 approx. 0.5-2.0 mm) spherical biofilms found in anaerobic digesters used to treat 2 industrial wastewaters, where they underpin efficient organic waste conversion and 3 biogas production. A single digester contains millions of individual granules, each of 4 which is a highly-organised biofilm comprised of a complex consortium of likely 5 billions of cells from across thousands of speciesbut not all granules are identical. 6Whilst each granule theoretically houses representative microorganisms from all of 7 the trophic groups implicated in the successive and interdependent reactions of the 8 anaerobic digestion process, parallel granules function side-by-side in digesters to 9 provide a 'meta-organism' of sorts. Granules from a full-scale bioreactor were size-10 separated into small, medium and large granules. Laboratory-scale bioreactors were 11 operated using only small (0.6-1 mm), medium (1-1.4 mm) or large (1.4-1.8 mm) 12 granules, or unfractionated (naturally distributed) sludge. After >50 days of 13 operation, the granule size distribution in each of the small, medium and large 14 bioreactor types had diversified beyondto both bigger and smaller thanthe size 15 fraction used for inoculation. 'New' granules were analysed by studying community 16 structure based on high-throughput 16S rRNA gene sequencing. Methanobacterium, 17Aminobacterium, Propionibacteriaceae and Desulfovibrio represented the majority of 18 the community in new granules. H2-using, and not acetoclastic, methanogens 19 appeared more important, and were associated with abundant syntrophic bacteria. 20Multivariate integration analyses identified distinct discriminant taxa responsible for 21 shaping the microbial communities in different-sized granules, and along with alpha 22 diversity data, indicated a possible biofilm life cycle. 23Importance. Methanogenic granules are spherical biofilms found in the built 24 environment, where despite their importance for anaerobic digestion of wastewater 25

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Importance of Species Sorting and Immigration on the Bacterial Assembly of Different-Sized Aggregates in a Full-Scale Aerobic Granular Sludge Plant

Cited by 104 publications

References 62 publications

Size Shapes the Active Microbiome of Methanogenic Granules, Corroborating a Biofilm Life Cycle

Size Shapes the Active Microbiome of Methanogenic Granules, Corroborating a Biofilm Life Cycle

Island biogeography on a micro-scale: Larger anammox granules not only harbor higher species diversity but also support more functional diversity

De NovoGrowth of Methanogenic Granules Indicates a Biofilm Life-Cycle with Complex Ecology

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