Influence of alternate wetting and drying water-saving irrigation practice on the dynamics of Gallionella-related iron-oxidizing bacterial community in paddy field soil

Highlights

• This study focused on Gallionella-related Fe(II)-oxidizing bacteria (FeOB).

• AWD irrigation influenced the community structure of Gallionella-related FeOB.

• Their abundances negatively correlated with the Fe(II) contents in the soil.

• Their estimated contribution to the soil Fe(II) oxidation was 4.6%.

Abstract

The redox cycle of iron (Fe) is a key process in the biogeochemistry of paddy field soil. It has been recently remarked that Fe(II)-oxidizing bacteria belonging to the family Gallionellaceae (Gallionella-related FeOB) are one of the key players in the Fe(II) oxidation in the soil. The present study aimed to investigate the influence of alternate wetting and drying (AWD) irrigation for water-saving rice cultivation on the dynamics of the community of Gallionella-related FeOB in the paddy field soil over three seasons (wet-dry-wet seasons) of rice cultivation. The AWD irrigation brought about the reduction of Fe(II) contents in the soil, compared with the continuously flooding (CF) irrigation, especially in the last half of the rice cultivation period in the dry season. In contrast, a trend of higher copy number of 16S rRNA genes of Gallionella-related FeOB was observed in the last half of the rice cultivation period of the AWD paddy soil. As a result, a significant negative correlation was observed between the Fe(II) contents and the copy numbers of 16S rRNA genes. PCR-DGGE analysis of 16S rRNA genes of Gallionella-related FeOB showed that the band patterns were different between the CF and AWD paddy soils. Meanwhile, the results of clone library analysis indicated that differences in the taxonomic composition of Gallionella-related FeOB were not observed between the CF and AWD paddy soils, suggesting that Gallionella-related FeOB responded to the AWD water-saving irrigation on the individual strain levels. The potential of Fe(II)-oxidizing activity and its apparent contribution of the activity of Gallionella-related FeOB to the Fe(II) oxidation in the soil of the investigated field were estimated to be 2.4 × 10⁻³ to 1.7 × 10⁻¹ mg Fe(II) g⁻¹ dry soil day⁻¹ and 4.6%, respectively, based on the reported Fe(II) oxidation rates of cells. The present study showed that the fluctuation of the redox status of Fe caused by the repeated cycle of wetting and drying of the field brought about the changes in the community structure of Gallionella-related FeOB in the soil. Furthermore, it was suggested that Gallionella-related FeOB were certainly involved in the Fe(II)-oxidizing process in the AWD paddy field soil.

Introduction

Iron (Fe), which comprises approximately 5% (w/w) in the lithosphere (Kabata-Pendias, 2000), occurs mainly between oxidized (i.e. ferric Fe, Fe(III)) and reduced (i.e. ferrous Fe, Fe(II)) states in environments. Various processes including microbial and chemical reactions mediate both the reduction and oxidation of Fe in environments, and the ecophysiological roles of Fe(II)-oxidizing bacteria have been recently highlighted (Melton et al., 2014) since several types of Fe(II)-oxidizing bacteria have been newly discovered from circumneutral environments in the 1990s (e.g. Widdel et al., 1993; Straub et al., 1996; Emerson and Moyer, 1997). Nowadays, three types of microbial Fe(II)-oxidizing reactions have been recognized in circumneutral environments: microaerophilic, phototrophic, and nitrate-reducing Fe(II) oxidation (Melton et al., 2014).

The redox cycle of Fe is a key process in the biogeochemistry of paddy field soil. Although chemical Fe(II) oxidation had been considered as the predominant reaction in paddy soils, the importance of microbial Fe(II) oxidation has become recognized recently with increase in interest. Some studies have reported nitrate-reducing Fe(II) oxidation (Murase and Kimura, 1997; Klüber and Conrad, 1998; Ratering and Schnell, 2001; Li et al., 2016; Liu et al., 2019), which showed a potential of nitrate-reducing Fe(II) oxidation in paddy field. To extrapolate the possible niches for microaerophilic Fe-oxidizing bacteria (FeOB), the oxygen (O₂) and Fe(II) gradients in the rice rhizosphere microsites were analyzed (Maisch et al., 2019a). Furthermore, the involvement of FeOB in the family Gallionellaceae (Gallionella-related FeOB) in the Fe(II) oxidation has been reported recently. Gallionella ferruginea, the type species and genus of Gallionella and Gallionellaceae, has been one of the typical microaerophilic Fe oxidizers inhabiting circumneutral freshwater environments since early times (Hedrich et al., 2011), and all the other species in Gallionella-related FeOB, Ferriphaselus amnicola (Kato et al., 2014), ‘Ferriphaselus globulitus’ (Krepski et al., 2012; Kato et al., 2015), ‘Sideroxydans lithotrophicus’ (Emerson and Moyer, 1997; Weiss et al., 2007; Emerson et al., 2013), ‘Gallionella capsiferriformans’ (Emerson and Moyer, 1997; Emerson et al., 2013), and ‘Sideroxydans paludicola’ (Weiss et al., 2007), have also been known as microaerophiles with an exception that a Gallionellaceae sp. in the enrichment culture KS is capable of oxidizing Fe(II) by reducing nitrate (He et al., 2016). Khalifa et al. (2018) described a novel microaerophilic Fe oxidizer, Ferrigenium kumadai An22 belonging to the family Gallionellaceae, which was isolated from a Fe oxide-deposited microbial colony formed on the paddy soil surface (Watanabe et al., 2013b). The results of the community analysis of Gallionella-related FeOB suggested the inhabitance of a considerable number of diverse Gallionella-related FeOB in paddy field soils and showed a negative correlation between the abundance of Gallionella-related FeOB and Fe(II) contents during a rice cultivation period (Naruse et al., 2019). An increase in the abundance of Gallionella-related FeOB was observed in the surface oxic layer of a flooded paddy field soil (Nakagawa et al., 2020). These previous studies suggested that nitrate-reducing and microaerophilic Fe(II) oxidation occurs, and Gallionella-related FeOB are one of the key players in the microbial Fe(II) oxidation in paddy field soils.

A paddy field is a distinct agroecosystem, compared with other upland agroecosystems. Rice is generally cultivated under flooded conditions with irrigation water or rainwater. Meanwhile, the field is drained briefly even during rice cultivation in some situations (e.g. midsummer drainage) and before rice harvesting. As a result, the redox conditions in the soil fluctuate depending on the moisture conditions. The regulation of water level in the field is an important factor for rice growth, and also to regulate the soil redox conditions and mitigate the methane emission (e.g. Le Mer and Roger, 2001; Tirol-Padre et al., 2018; Yagi et al., 2020), to reduce the absorption of harmful elements by rice (e.g. Arao et al., 2010), and to save the water usage (e.g. Bouman et al., 2007). Alternate wetting and drying (AWD) irrigation has been introduced as one of the ways to save water usage for rice cultivation in several countries (Lampayan et al., 2015). The principal of the AWD irrigation is to irrigate the field only when the soil water conditions, e.g. water potential or water level, decrease to a criterion except for some periods when rice needs a copious amount of water for the growth. Accordingly, the water usage was reduced by up to 38% without a decrease in the rice yield (Lampayan et al., 2015).

Since the field is repeatedly irrigated and drained, the AWD water-saving practice must influence various biogeochemical processes in paddy field soil (e.g. methane emission [Yagi et al., 2020]). The fluctuation of soil moisture conditions must bring about the frequent changes in the redox status of Fe in the soil. However, the influence of AWD water-saving practice on the dynamics of FeOB has not been investigated yet. We hypothesized that the frequent changes in the redox status of Fe give occasions for Gallionella-related FeOB to participate in the Fe(II) oxidation and proliferate in the soil. In the present study, therefore, the dynamics of the community structure of Gallionella-related FeOB and their response to the changes in the redox status of Fe in the paddy field soil were analyzed in the AWD water-saving paddy field soils over three seasons of rice cultivation.