Recurring heavy rainfall resulting in degraded-upgraded phases in soil microbial networks that are reflected in soil functioning

Highlights

● We assess the recovery of microbial networks underneath crust to repeated rainfall.

● The network fragmentation after the second heavy rain was milder than at the first one.

● Cohesive networks were related to high enzyme activity involved in C, N, and P cycles.

● Loose networks were related to high Ca, K, Mg, NH₄ and organic N.

● The network in dry-crusted soils collapsed after the second heavy rain.

Abstract

Biological soil crusts (BSCs) are an important multi-trophic component of arid ecosystems in the Mediterranean region. In a mesocosm experiment, the authors investigated how the network of interactions among the members of the soil microbial communities in four types of soil sample responded when soils were exposed to two simulated extreme rain events. The four types of soil samples were: covered by Cladonia rangiformis and previously hydrated (+BSC+H), covered by C. rangiformis and dried (+BSC-H), uncovered and hydrated (-BSC+H), uncovered and dried (-BSC-H). Network analysis was based on the co-occurrence patterns of microbes; microbes were assessed by the phospholipid fatty acids analysis. The authors further explored the relations between networks’ metrics and soil functions denoted by enzymatic activity and soil chemical variables. All networks exhibited Small world properties, moderate values of clustering coefficient and eigen centrality, indicating the lack of hub nodes. The networks in -BSC-H soils appeared coherent during the pre-rain phases and they became modular after rains, while those in +BSC-H soils kept their connectivity till the second rain but this then collapsed. The network metrics that were indicative of cohesive networks tended to be related to enzyme activity while those that characterized the loose networks were related to Ca, K, Mg, NH₄⁺ and organic N. In all mesocosms except for +BSC-H, networks’ fragmentation after the second heavy rain was milder than after the first one, supporting the idea of community acclimatization. The response of microbial networks to heavy rains was characterized by the tendency to exhibit degradation-reconstruction phases. The network collapse in the crusted only mesocosms showed that the communities beneath crusts in arid areas were extremely vulnerable to recurring heavy rain events.

Graphical abstract

Keywords

PLFAs / Cladonia rangiformis / biocrust / soil microbial community / network metrics

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Abbreviations

NAG: N-acetyl-glycosaminidase

BG: b-glucosidase

AP: acid phosphomoesterase

UREA: urease

PPO: polyphenol oxidase

SOC: soil organic carbon

SON: soil organic N

EC: eigen centrality

L: shortest path

CC: clustering coefficient

Fr: fragmentation

SW: Small-worldness

Deg: Degree centrality

Acknowledgements

Open access funding provided by HEAL-Link Greece.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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