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Downloaded from the NCBI Genome Repository ORIGINAL RESEARCH published: 07 July 2020 doi: 10.3389/fmicb.2020.01637 Comparative Genome-Centric Analysis of Freshwater and Marine ANAMMOX Cultures Suggests Functional Redundancy in Nitrogen Removal Processes Muhammad Ali 1, Dario Rangel Shaw 1, Mads Albertsen 2 and Pascal E. Saikaly 1* 1 Water Desalination and Reuse Center (WDRC), Biological and Environmental Science & Engineering (BESE), King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia, 2 Center for Microbial Communities, Aalborg University, Aalborg, Denmark There is a lack of understanding of the interaction between anammox bacteria and the flanking microbial communities in both freshwater (non-saline) and marine (saline) ecosystems. Here, we present a comparative genome-based exploration of two different anammox bioreactors, through the analysis of 23 metagenome-assembled genomes (MAGs), 12 from freshwater anammox reactor (FWR), and 11 from marine anammox Edited by: reactor (MWR). To understand the contribution of individual members to community Simona Rossetti, functions, we applied the index of replication (iRep) to determine bacteria that are Water Research Institute (CNR), Italy actively replicating. Using genomic content and iRep information, we provided a Reviewed by: Jin Li, potential ecological role for the dominant members of the community based on the Qingdao University, China reactor operating conditions. In the non-saline system, anammox (Candidatus Brocadia Daan R. Speth, sinica) and auxotrophic neighboring bacteria belonging to the phyla Ignavibacteriae California Institute of Technology, United States and Chloroflexi might interact to reduce nitrate to nitrite for direct use by anammox *Correspondence: bacteria. Whereas, in the saline reactor, anammox bacterium (Ca. Scalindua erythraensis) Pascal E. Saikaly and flanking community belonging to phyla Planctomycetes (different than anammox [email protected] bacteria)—which persistently growing in the system—may catabolize detritus and Specialty section: extracellular material and recycle nitrate to nitrite for direct use by anammox bacteria. This article was submitted to Despite different microbial communities, there was functional redundancy in both Microbiotechnology, a section of the journal ecosystems. These results signify the potential application of marine anammox bacteria Frontiers in Microbiology for treating saline N-rich wastewaters. Received: 28 April 2020 Keywords: biological nitrogen removal, anammox, Candidatus Scalindua, saline wastewaters, genome-resolve, Accepted: 23 June 2020 nanopore sequencing, Candidatus Brocadia Published: 07 July 2020 Citation: Ali M, Shaw DR, Albertsen M and INTRODUCTION Saikaly PE (2020) Comparative Genome-Centric Analysis of Microbial communities are an abundant natural resource that represents functional biological Freshwater and Marine ANAMMOX Cultures Suggests Functional entities with diverse metabolic capacities. Various strategies have been used to optimize the Redundancy in Nitrogen Removal management of microbial resources to tailor the needs of specific applications (Rittmann et al., Processes. Front. Microbiol. 11:1637. 2006). Biological wastewater treatment systems are the most common large-scale examples of these + doi: 10.3389/fmicb.2020.01637 strategies where microbes remove organic and inorganic pollutants, including ammonium (NH4 ), Frontiers in Microbiology | www.frontiersin.org 1 July 2020 | Volume 11 | Article 1637 Ali et al. Functional Redundancy in Anammox Cultures from wastewaters. Anaerobic ammonium-oxidizing (anammox) and neighboring microbial communities in engineered and bacteria capable of oxidizing ammonium to dinitrogen (N2) natural ecosystems (Lawson et al., 2017). A genome-centric − gas using nitrite (NO2 ) as a terminal electron acceptor are metagenome approach was employed to gain a comprehensive considered as one of the most energy-efficient biological nitrogen insight into the function of the entire microbial community + removal technologies for the treatment of NH4 -rich wastewater in various non-saline anammox bioreactors (Speth et al., 2016; streams (Ali and Okabe, 2015). Lawson et al., 2017). Typically, anammox bioreactors contain Besides, anammox process is a critical part of the global mixed microbial communities. These studies enhanced our nitrogen cycle and is detected in nearly all anoxic ecosystems understanding on metabolite exchange reactions pertaining to containing fixed nitrogen (Humbert et al., 2010). Anammox nitrogen cycle (nitrate recycling) and interaction of anammox bacteria are responsible for up to 50% of the biogeochemical bacteria with autotrophic nitrifying bacteria (Speth et al., 2016) N2 production in different ecosystems including marine and heterotrophic bacteria (Lawson et al., 2017) in non- environments (Dalsgaard et al., 2005, 2013; Xi et al., 2016), saline anammox-based bioreactors. Marine anammox bacteria + deep-sea hydrothermal vents (Byrne et al., 2009), marine could be a promising alternative for the treatment of NH4 - seagrass (Garcias-Bonet et al., 2018), groundwater (Moore rich saline industrial and/or municipal wastewater (Ali et al., et al., 2011), paddy soils (Zhu et al., 2011), lakes (Schubert 2020). Previously, we reported the enrichment of anammox et al., 2006), and estuaries (Trimmer et al., 2003). More than culture in a membrane bioreactor (MBR) capable of treating + 30 anammox species, divided among five candidate genera to treat NH4 -rich wastewater under moderate salinity and in within the Planctomycetes phylum have been detected in non- the presence of organic carbon (Ali et al., 2020). However, saline engineered and natural ecosystems, and marine (saline) little is known about the microbial community and the environments (Ali and Okabe, 2015). The anammox bacteria syntrophic cooperation between the microbial community of belonging to genera Kuenenia, Brocadia, Anammoxoglobus, saline anammox-based bioreactors. and Jettenia predominantly found in freshwater ecosystems We, therefore, hypothesized that even though marine and and the bacteria belonging to genus Scalindua are primarily freshwater environments harbor totally different communities, found in marine ecosystems (Sonthiphand et al., 2014). Distinct we expect to find functional redundancy in the nitrogen removal partitioning of anammox bacterial communities among natural process in saline and non-saline anammox reactors. Functional and engineered ecosystems have been observed, and it has been redundancy enables functional resistance of an ecosystem to postulated that the global distribution pattern of anammox environmental perturbations due to the presence of multiple bacteria is governed primarily by salinity (Sonthiphand et al., species that can perform the same metabolic function (e.g., 2014), their kinetic characteristics (Dale et al., 2009; Sonthiphand phosphorous removal, ammonium oxidation, nitrite oxidation, et al., 2014), and better aggregation ability (Ali et al., 2018). etc.) such that the loss of one species due to perturbation will Metagenomic analysis has been used to understand distant be substituted by another species in the community (Saikaly partitioning of anammox bacterial communities using draft and Oerther, 2011; Louca et al., 2018). In this study, we mainly genome encoded genetic content of the species. Previous focused on functional redundancy in terms of nitrogen removal metagenomic sequencing efforts have yielded draft near- processes of phylogenetically distant anammox bacteria in saline complete genome assemblies of eight different anammox species and non-saline ecosystems. To test this hypothesis, we performed (Gori et al., 2011; Speth et al., 2012, 2017; van de Vossenberg a genome-centric metagenome analysis of two physiologically et al., 2013; Oshiki et al., 2015; Ali et al., 2016a, 2019; Park distant (i.e., freshwater and marine) anammox-based bioreactors. et al., 2017), and one complete genome assembly for Ca. Four months’ time-series short-read sequencing data of both Kuenenia stuttgartiensis (Frank et al., 2018). Some comparative cultures were de novo assembled, and used for differential metagenomics studies have been performed on separately coverage binning to identify contigs belonging to the same enriched anammox communities (Speth et al., 2012), different microbial genome (Albertsen et al., 2013; Nielsen et al., microbial aggregates sizes (Guo et al., 2016), and lab-scale 2014). It is a challenge to assemble a complete or closed reactor configurations (Bhattacharjee et al., 2017) under non- genome from a metagenome sequencing data provided by saline conditions. Similarly, metagenomics studies have also been 2nd generation sequencing platforms (e.g., Illumina). Biases performed for saline environments in natural marine ecosystems and artifacts introduced during inherent DNA amplification (van de Vossenberg et al., 2013; Speth et al., 2017). However, steps often lead to fragmented genome coverage. Besides, the these aforementioned studies did not adopt a genome-centric relatively short read lengths prevent the resolution of large metagenomics approach but instead relied on a global analysis genomic repeats, highly similar paralogs, and other structural of genes and pathways. Genome-centric metagenomics approach variations by the assembler, leaving the assembly incomplete enables us to infer actual contribution of certain genome(s)toa (Eid et al., 2009). Repeat elements constrain the assembly specific metabolic pathway. contiguity of the genomes assembled from
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