A unique bacterial and archaeal diversity make mangrove a green production system compared to rice in wetland ecology: A metagenomic approach

Highlights

• Higher bacterial diversity was noticed in rice than degraded-mangrove in wetlands.

• Proteobacteria and Chloroflexi were the dominant group in degraded mangrove system.

• Lower GWP with higher labile C build-up potential makes mangrove a green system than rice.

• Higher the ratios of methanotrophs/SRB:methanogens in mangrove than rice reduced GHGs emissions.

Abstract

Mangrove provides significant ecosystem services, however, 40% of tropical mangrove was lost in last century due to climate change induced sea-level rise and anthropogenic activities. Sundarban-India, the largest contiguous mangrove of the world lost 10.5% of its green during 1930–2013 which primarily converted to rice-based systems. Presently degraded mangrove and adjacent rice ecology in Sundarban-India placed side by side and create typical ecology which is distinct in nature in respect to soil physicochemical properties, carbon dynamics, and microbial diversities. We investigated the structural and functional diversities of bacteria and archaea through Illumina MiSeq metagenomic analysis using V3–V4 region of 16S rRNA gene approach that drives greenhouse gases emission and carbon-pools. Remote sensing-data base were used to select the sites for collecting the soil and gas samples. The methane and nitrous oxide emissions were lower in mangrove (−0.04 mg m⁻² h⁻¹ and −52.8 μg m⁻² h⁻¹) than rice (0.26 mg m⁻² h⁻¹ and 44.7 μg m⁻² h⁻¹) due to less availability of carbon-substrates and higher sulphate availability (85.8% more than rice). The soil labile carbon-pools were more in mangrove, but lower microbial activities were noticed due to stress conditions. A unique microbial feature indicated by higher methanotrophs: methanogens (11.2), sulphur reducing bacteria (SRB): methanogens (93.2) ratios and lower functional diversity (7.5%) in mangrove than rice. These could be the key drivers of lower global warming potential (GWP) in mangrove that make it a green production system. Therefore, labile carbon build-up potential (38%) with less GWP (63%) even in degraded-mangrove makes it a clean production system than wetland-rice that has high potential to climate change mitigation. The whole genome metagenomic analysis would be the future research priority to identify the predominant enzymatic pathways which govern the methanogenesis and methanotrophy in this system.

Introduction

Mangrove covers around 60–70% of tropical and subtropical coastlines wetlands of the world and provides significant ecological services (Ghosh et al., 2010; Padhy et al., 2020). Sundarban is one of the largest contiguous mangroves in the world situated in the delta of three major rivers (Ganga, Meghna and Brahmaputra). The total Sundarban mangrove area is around 10,000 km², out of which 38% is in India and rests in Bangladesh (Spalding et al., 2010). Mangrove ecosystem plays a key role in carbon (C) dynamics, energy flow and nutrient cycling in wetland coastal ecosystems (Ghizelini et al., 2012; Zeng et al., 2014; Priya et al., 2018). However, 40% of tropical mangrove was ecologically degraded in the last century (Padhy et al., 2020). Moreover, climate change induced sea-level rise and indiscriminate anthropogenic activities still causing soil degradation in Sundarban, India. Several parts of mangrove wetlands in Sundarban have been converted to agricultural sector mainly to rice and aquaculture since the last century. Hence, the mangrove-rice interphases create a typical ecology having specific soil physicochemical characteristics, C-dynamics, and greenhouse gases (GHGs) emissions which are distinct in nature.

Mangrove and rice are typically providing passage to GHGs emission, mainly methane (CH₄) and nitrous oxide (N₂O) from soil to the atmosphere through pneumatophore and rice-aerenchyma columns, respectively (Bhattacharyya et al., 2020). Methane emission depends on both the natural and anthropogenic factors; especially the soil carbon pools, anoxic conditions, and microbial diversity.

The labile soil C pools could be selected as sensitive indicators (Tian et al., 2013) to determine the C dynamics in degraded mangrove ecologies. Similarly, in the rice rhizosphere, the soil labile C pools play an important role in enhancing microbial metabolic activities. Soil labile C pools mainly represented by microbial biomass C (MBC), water soluble C (WSC), readily mineralizable C (RMC), dissolved organic C (DOC), and potassium permanganate oxidizable C (KMnO₄-C), are often used as indicators for soil quality assessment in wetlands like mangrove and lowland rice ecologies (Wohlfart et al., 2012; Padhy et al., 2020). Studies have indicated that the labile C fractions are significantly associated with the GHGs emission and nutrient availability of soils and small changes of which could be detected precisely (Wohlfart et al., 2012).

The anoxic condition of tidal plain in presence of high organic C creates a favorable condition for sulphate-reducing bacteria (SRB) and methanogens (Dar et al., 2008). Salinity increases the availability of terminal electron acceptors, which could shift the microbial metabolism towards higher energetically favorable sulphate reduction processes than CH₄ production (Neubauer, 2013). Sulphur reduction usually takes place at lower redox potential as compared to methanogenesis. So, sulphur reduction took place before CH₄ production and continues till the sulphate ions available in the soil and redox potential (Rh) reduced to -200mv. Therefore, the high sulphate availability in mangrove could reduce the CH₄ production rates. Additionally, oxidation of CH₄ at near-surface due to tidal influence also slows down the CH₄ emissions.

Microbial functional as well as structural diversities are associated with the GHGs emission and C-dynamics in mangrove-rice ecosystems. A diverse group of microorganisms are generally observed in the rice rhizospheric soil due to the availability of substrate through root exudation, residue decomposition and application of fertilizer which are distinctly different from typical mangrove-ecologies (Bhattacharyya et al., 2016). Both the mangrove and rice plants could oxidize the soil by supplying oxygen to the anaerobic rhizospheric region through their roots (Wu et al., 2016). Several bacteria and archaea communities related to GHGs emissions, such as methanogens, methanotrophs, nitrifiers, denitrifiers, sulphate-reducing bacteria, etc. play a significant role in mangrove as well as rice ecologies. Further, soil-enzymatic activities like dehydrogenase (DHA), fluorescein diacetate (FDA) and β-glucosidase (β-GLU) are effective ecological indicators of soil microbial functional diversities (Wang and Li, 2014; Bhattacharyya et al., 2016, Bhattacharyya et al., 2020). Metagenomic analysis of soil bacteria and archaea could give valuable insight of the structural feature and microbial functionality of the system related to GHGs emissions and C-dynamics. Considering the above mention issues, we framed two objectives of this study; (i) to study the structural and functional soil-bacterial diversities in degraded mangrove and adjacent rice ecologies through metagenomic approach, and (ii) to estimate and correlate the GHGs emissions with soil labile C pools and microbial diversities in mangrove-rice interphases.