Genomic adaptation to eutrophication of ammonia‐oxidizing archaea in the Pearl River estuary

Abstract

Summary Ammonia‐oxidizing archaea (AOA) are ubiquitous in natural ecosystems, and they are responsible for a significant fraction of ammonia oxidation globally. Since the first AOA isolate was established a decade ago, molecular surveys of their environmental distribution [based primarily on amplicon sequencing of the amoA, which codes for the alpha subunit of ammonia monooxygenase (AMO)], show that their habitats are believed to range from marine to terrestrial environments. However, the mechanisms of adaptation underpinning to their habitat expansion remain poorly understood. Here, we report that AOA accounts for almost all of the ammonia oxidizers in the shelf water adjacent to the Pearl River estuary (PRE), with the Nitrosopumilus maritimus SCM1‐like (SCM1‐like) being the main amoA genotype. Using a metagenomic approach, seven high‐quality AOA genomes were reconstructed from the PRE. Phylogenetic analysis indicated that four of these genomes with high completeness were closely affiliated with the Nitrosomatrinus catalina strain SPOT01, which was originally isolated off the coast of California. Genomic comparison revealed that the PRE AOA genomes encoded genes functioning in amino acid synthesis, xenobiotic biodegradation metabolism and transportation of inorganic phosphate and heavy metals. This illustrates the different adaptations of AOA in one of the largest estuaries in China, which is strongly influenced by anthropogenic input. Overall, this study provides additional genomic information about estuarine AOA and highlights the importance of their contribution to nitrification in eutrophic coastal environments.

Community, Distribution, and Ecological Roles of Estuarine Archaea

“…AOA are suggested as major players in the nitrogen cycle in low-nutrient environments ( Erguder et al, 2009 ), such as the oligotrophic oceans ( Francis et al, 2005 ). They are also reported as the major ammonia oxidizers in some eutrophic estuaries ( Beman and Francis, 2006 ; Bernhard and Bollmann, 2010 ; Cao et al, 2011 ; Jin et al, 2011 ; Wang et al, 2014 ; Zou et al, 2019 , 2020b ) and lakes ( Wu et al, 2010 ; Hou et al, 2013 ; Zhao et al, 2013 ; Bollmann et al, 2014 ). The impact of these environmental parameters, especially the salinity and ammonium concentration, on the distribution of AOA varies with species ( Fukushima et al, 2012 ; Hatzenpichler, 2012 ; Stahl and de la Torre, 2012 ), which implies that AOA are well adapted to different environments.…”

“…Increasing numbers of archaeal groups are being recognized as vital players in estuarine biogeochemical cycles ( Figure 1 ). These include: Thaumarchaeota , which comprise ammonia oxidizing archaea (AOA), one of the key players of ammonia oxidation in estuaries ( Francis et al, 2005 ; Liu L. et al, 2011 ; Liu Z. et al, 2011 ; Zou et al, 2019 , 2020b ); Bathyarchaeota (formerly called Miscellaneous Crenarchaeotal Group, MCG), which are hypothesized to be important players in the benthic carbon cycle that, based on genomic analysis, may be able to utilize diverse organic substrates ( Meng et al, 2014 ; Lazar et al, 2015 , 2016 ; He et al, 2016 ; Zhou et al, 2018a ); Euryarchaeota , e.g., most methanogens and anaerobic methanotrophs, are responsible for methane production and oxidation in estuaries, respectively ( Oremland and Polcin, 1982 ; Serrano-Silva et al, 2014 ); and Asgard archaea, such as Thorarchaeota and Lokiarchaeota , which may participate in some biogeochemical cycles, as suggested by metagenomics ( Seitz et al, 2016 ; Liu Y. et al, 2018 ; MacLeod et al, 2019 ; Cai et al, 2020 ). Recently, Liu et al (2018b) explored the diversity and community structure of archaea in over 20 estuaries.…”

“…Analyses of the archaeal amoA gene encoding the α-subunit of ammonia monooxygenase (AMO) revealed that archaea with an ammonia-oxidizing potential are ubiquitous in natural environments ( Francis et al, 2005 ; Biller et al, 2012 ; Cao et al, 2013 ; Cheung et al, 2019 ). Members of chemolithoautotrophic AOA may be mixotrophic, as they harbor genes encoding extracellular peptidases and carbohydrate-active enzymes ( Li et al, 2015 ; Zou et al, 2019 ). In addition, because of high affinity for ammonia, low oxygen demand, and tolerance of a wide salinity range, AOA are thought to have more prominent advantages for estuarine ammonia oxidation ( Bollmann and Laanbroek, 2002 ; Martens-Habbena et al, 2009 ; Mosier et al, 2012b ; Qin et al, 2017 ).…”

“…Light may also influence the AOA distribution. Archaeal AMO enzymes are more sensitive to photoinhibition than bacterial AMO enzymes ( Merbt et al, 2012 ), which leads to AOA enrichment in the bottom water layers of estuaries ( Zou et al, 2019 ). As another factor, temperature controls the diversity and distribution of AOA in the Westerschelde Estuary ( Sahan and Muyzer, 2008 ).…”

“…Phosphate usually limits the growth of aquatic microbes in estuarine and coastal regions. Accordingly, estuarine AOA reportedly have many genes related to phosphate transport and regulation systems related to phosphate acquisition ( Mosier et al, 2012b ; Zou et al, 2019 ). Alternatively, they may utilize diverse types of phosphorus sources by using polyphosphate enzymes and phosphatases ( Qin et al, 2020 ; Zou et al, 2020a ).…”